Original Article

Yonago Acta medica 2016;59:204–209

R2* Map by IDEAL IQ for Acute Cerebral Infarction: Compared with Susceptibility
Vessel Sign on T2*-Weighted Imaging
Yuki Shinohara,* Ayumi Kato,* Eijiro Yamashita† and Toshihide Ogawa**Division of Radiology, Department of Pathophysiological Therapeutic Science, School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8503, Japan and †Division of Clinical Radiology, Tottori University Hospital, Yonago 683-8504, Japan

ABSTRACTtion as early as possible because therapeutic strategies
are different depending on each pathophysiology.1, 2
T2*-weighted imaging (T2*WI) is a useful MR
sequences that enable to detect susceptibility effects
such as hemorrhage, calcifications, venous structures including tissue ischemic sign and acute emboli with highsensitivity.6–10 Recently, evaluating susceptibility effectof intra-arterial acute thrombus as susceptibility vessel
sign is considered to be critical because location, size, orsignal intensity of susceptibility vessel sign on T2*WI
are the important factors to predict the effectiveness ofthrombolytic therapy by intravenous recombinant tissue
plasminogen activator (rtPA) and mechanical thrombectomy with endovascular procedure.11–15
Although T2*WI has an advantage of detecting
acute thrombi as previously reported, it also has awell-established drawback of this sequence. The imageof T2*WI near the skull base can be distorted becauseof the strong susceptibility artifact, which may decrease
the detectability of susceptibility sign near the skull
base, such as distal internal carotid artery (ICA), basilar-top and proximal posterior cerebral artery (PCA)
segments.10–13
On the other hand, a newly developed multi-echo reconstruction technique, called R2* map, is an algorithm
based on 6-point Dixon method, which can correct T2*
decay and eddy currents induced phase errors.16–18 R2*
map can generate quantitative susceptibility-sensitive
image and we hypothesize that R2* map will have a potential to detect acute thrombus with high accuracy.
The purpose of the present study is to evaluate thedetectability of arterial fresh thrombus on R2* map

BackgroundTo evaluate the detectability of arterial
acute thrombus on R2* map by iterative decompositionof water and fat with echo asymmetry and least-squares
estimation (IDEAL) IQ compared with T2*-weighted
imaging (T2*WI).
Methods Twenty-six patients with acute cerebral
infarction who underwent R2* map and T2*WI werereviewed. We performed visual assessment of each sequence regarding the visibility of susceptibility effectreflecting acute thrombus and quantitative evaluation of
the thrombus on R2* map.
Results Both R2* map and T2*WI showed susceptibility effect reflecting acute thrombi at the occluded siteof magnetic resonance angiography (MRA) in 9 patients.
R2* map revealed positive while T2*WI showed equivocal findings in 3 patients due to the surrounding vessel
signal intensity. Acute thrombus at distal internal carotid
artery (ICA) on R2* map was more clearly detected
than that on T2*WI without any apparent susceptibility
artifact from the skull base in 4 patients. Most of cardiogenic embolic infarction (CEI) and artery-to-artery embolic infarction (A-to-A) demonstrated positive and mostof atherothrombotic infarction (ATI) revealed negative
findings on R2* map, although quantitative R2* valuesof thrombi did not show significant differences between
CEI (136.6 /msec) and A-to-A (189.9 /msec) (P = 0.332).
Conclusion The detectability of acute thrombus on
R2* map is comparable to that on T2*WI. Regarding
thrombus at distal ICA, its detectability on R2* map issuperior to that on T2*WI. R2* map provide additional
information to distinguish between embolic and atherothrombotic infarctions.

Corresponding author: Yuki Shinohara, MD
shino-y@olive.plala.or.jp
Received 2016 June 22
Accepted 2016 July 6
Abbreviations: ATI, atherothrombotic infarction; A-to-A, artery-to-artery embolic infarction; CEI, cardiogenic embolic infarction; DWI, diffusion weighted imaging; FOV, field of view; ICA,
internal carotid artery; IDEAL, iterative decomposition of waterand fat with echo asymmetry and least-squares estimation; MCA;
middle cerebral artery, MR, magnetic resonance; MRA, MR angiography; PCA, posterior cerebral artery; ROI, regions of interest;
rtPA, recombinant tissue plasminogen activator; TE, echo time; TR,
repetition time; T2*WI, T2*-weighted imaging

Key words

central nervous system; embolism/thrombosis; ischemia/infarction; magnetic resonance imaging
Magnetic resonance (MR) imaging plays an importantrole for acute cerebral infraction to investigate the presence of ischemic lesion, ischemic penumbra and hemorrhagic complication.1–6 In addition, it is important torecognize the causes of infarction including cardiogenic
embolism, atherosclerotic infarction, and lacunar infarc204

R2* map for acute cerebral infarction

compared with conventional T2*WI in the patients withacute cerebral infarction. To our knowledge, there were
only a few investigations to refer to the usefulness of
R2* map in the central nervous system disorders,19, 20
and this is the first report to examine the utility of R2*
map in acute cerebral infarction.

this study (approval number 2582), and waived the need
for written informed consent because of its retrospective
design.
Imaging examinations

All MR examinations were performed using a 3T MR
system (Discovery MR750w 3.0 T, GE Healthcare,
Milwaukee, WI). R2* map is one of the sequences generated by single scanning of IDEAL IQ. Each scanningparameter of IDEAL IQ for R2* map, T2*WI, DWI and
MRA was as follows: IDEAL IQ: repetition time (TR),
8.3 ms; echo time (TE), six different echoes ranging
from 1.2 to 7.2 ms; field of view (FOV), 21 cm; matrix,
256 × 256; slice thickness, 2.0 mm, acquisition time, 1
min 47 s. T2*WI: TR, 600 ms; TE, 18 ms; FOV, 21 cm;
matrix, 512 × 512; slice thickness, 5.0 mm; acquisitiontime, 1 min 5 s. DWI: TR, 7,000 ms; FOV, 21 cm; matrix, 128 × 128; slice thickness, 5.0 mm. MRA: TR, 20
ms; TE, 3.4 ms; FOV, 20 cm; matrix, 384 × 224; slice
thickness, 1.0 mm.

MATERIALS AND METHODSPatients

This retrospective study analyzed data obtained from all
patients with a stroke admitted to our institution between
April 2, 2013 and September 30, 2014. Patients were eligible if they met the following criteria: MR imaging including diffusion weighted imaging (DWI), T2*WI, R2*
map by iterative decomposition of water and fat withecho asymmetry and least-squares estimation (IDEAL)
IQ and 3 dimensional time of flight MR angiography(MRA) performed, at least one occluded intracranial
vessel on initial MRA, and cause of brain infarction
with intracranial vessel occlusion confirmed from clinical information. Our institutional review board approved

Table 1. The summary of clinical data and the results of our study in 26 patientsInterval between initial MR imag- Cause of brain
Patient Age (years) ing
and symptom onset (hours)
infarction/sex

Imaging findings
Affected vessel on T2*WI
MRA

R2* map

Mean R2*
value(/msec)

1
81/M
7
CEI
Rt. terminal ICA Positive
Positive147.78
2
89/F
2.5
CEI
Lt. terminal ICA Not evaluable
Positive
240.9
3
70/M
3
CEI
Lt. ICANot evaluable
Positive269.26
480/F
6CEI
Rt. M1
Positive
Positive
169.95
582/M
6CEI
Rt. M1
Negative
Negative
–
6
82/M
1.5
CEI
Lt. M1
Equivocal
Positive142.36
7
76/F
3.5
CEI
Rt. M2
Positive
Positive107.08886/F
6CEI
Rt. M2
Positive
Positive
66.39
9
93/F
8
CEI
Rt. M2Equivocal
Positive
65.7
10
76/F
2
CEI
Lt. M2
Positive
Positive
62.83
11
58/F
4
CEI
Lt. M2
Positive
Positive146.53
12
58/M
4
CEI
Lt. M2
Positive
Positive155.39
13
56/M
7
CEI
Lt. PICA
Equivocal
Positive
64.73
14
61/M
24
A-to-A
Rt. ICANot evaluable
Positive122.75
15
66/M
22
A-to-A
Lt. ICANot evaluable
Positive
317.71
16
83/M
18
A-to-A
Lt. M1
Positive
Positive
194.8917
71/M
7
A-to-A
Lt. M2
Positive
Positive124.12
18
67/M
4
A-to-A
Lt. PICA
Negative
Negative
–
19
63/M
3
ATI
Rt. M1
Negative
Negative
–
20
68/M
24
ATI
Rt. M1
Equivocal
Negative
–
21
75/F
1.5
ATI
Rt. M1
Equivocal
Equivocal
–
22
58/M
1
ATI
Lt. M1
Negative
Negative
None
23
67/M
18
ATI
Lt. M1
Negative
Negative
None
24
82/M
20
ATI
Rt. M2
Negative
Negative
None
25
84/F
20
ATI
BA
Negative
Negative
None
26
77/F
2.5
ATI
Lt. PCA
Equivocal
Negative
None
ATI, atherothrombotic infarction; A-to-A, artery-to-artery embolic infarction; BA, basilar artery; CEI, cardiogenic embolic infarction;
F, female; ICA, internal carotid artery; lt., left; M, male; MR, magnetic resonance; MRA, MR angiography; M1, horizontal segment of
MCA; M2, insular segment of MCA; PICA, posterior inferior cerebellar artery; rt., right; T2*WI, T2*-weighted imaging.

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Y. Shinohara et al.

Image analysis

We performed visual assessment of R2* map and T2*WI at steno-occluded site of MRA. We divided 4 categories according to the consensus of the 2 neuroradiologists (Y.S. and A.K., with 12 and 4 years of experience,
respectively, in diagnostic neuroradiology) as follows:i) positive = definitely visible of susceptibility effectreflecting thrombi; ii) negative = definitely invisible ofsusceptibility effect reflecting thrombi; iii) equivocal= difficult to distinguish between susceptibility effectreflecting thrombi and other paramagnetic substances,and iv) not evaluable = difficult to evaluate susceptibility
effect reflecting thrombi due to susceptibility artifacts
arising from skull base.
We also performed quantitative assessment of acutethrombi on R2* map. Regions of interest (ROI) were
defined as areas of susceptibility effect reflecting thrombi on R2* map and mean R2* values of thrombi were
measured in each patient. Each difference of R2* value
among stroke subtypes was analyzed with Mann-Whitney U test using SPSS software (version 19.0; SPSS,
Chicago, IL). A P value < 0.05 was considered statistically significant.

while T2*WI showed equivocal findings due to the surrounding vessel signal intensity of thrombus in 3 patientswith CEI (Fig. 2). Acute thrombus in terminal ICA on
R2* map is more clearly detected than that on T2*WI (notevaluable) without any apparent susceptibility artifact
from the skull base around thrombus in 2 patients with
CEI and 2 patients with A-to-A (Fig. 3).
Both R2* map and T2*WI indicated negative findings corresponding to the occluded site of MRA in 1
patient with CEI, 1 patient with A-to-A and 5 patientswith ATI. R2* map showed negative findings, whereas
T2*WI demonstrated slight hypointensity which mightreflect the other paramagnetic substances such as artery
itself or arterial wall calcification in 2 patients with ATI.
The other 1 patient had equivocal finding on both R2*
map and T2*WI.
For quantitative assessment of susceptibility effect ofthrombi, we could trace the margin of emboli as ROI for
measuring R2* values (1/T2*, /msec) in 12 of 13 patientswith CEI and 2 of 4 patients with A-to-A. Mean R2*
values of CEI and A-to-A were 136.6 /msec and 189.9 /
msec, respectively. There were no significant differences
between them (P = 0.332).

RESULTS
Twenty-six patients (16 men and 10 women; mean age,
73 years; range, 56–93 years) were enrolled in the present study. The causes of brain infarction with intracranial vessel occlusion were as follows: 13 of cardiogenic
embolic infarction (CEI), 5 of artery-to-artery embolic
infarction (A-to-A), and 8 of atherothrombotic infarction(ATI). A summary of our results is shown in Table 1.
Both R2* map and T2*WI showed susceptibility
effect reflecting acute thrombi at the occluded site of
MRA in 7 patients with CEI and 2 patients with A-to-A(Fig. 1). R2* map enabled to show positive findings

DISCUSSION
Our results showed that R2* map demonstrated acutethrombus as prominent susceptibility effect with highsensitivity in the patients of CEI and A-to-A embolism.
In addition, R2* map could demonstrate susceptibility
effect of ICA embolus, which are difficult to detect onconventional T2*WI due to the strong susceptibility
artifact arising from the skull base.10, 13 Although quantitative R2* values of thrombi showed no significant
difference between CEI and A-to-A, R2* map showednegative findings at occluded sites in ATI so that it waspossible to distinguish between embolic and athero-A

Y. Shinohara et al. P. 24

B

Y. Shinohara et al. P. 25

C

Y. Shinohara et al. P. 26

D

Y. Shinohara et al. P. 27

Fig. 1. 80-year-old female with CEI in the right MCA territory (patient 4).
DWI shows restrict diffusion in the right basal ganglia (A) and MRA reveals occlusion at horizontal segment of right MCA (B). Corresponding to the occlusion site of MRA, both T2*WI (C) and R2* map (D) show prominent susceptibility effect reflecting fresh thrombus(→). CEI, cardiogenic embolic infarction; DWI, diffusion weighted imaging; MCA, middle cerebral artery; MRA, magnetic resonanceangiography; T2*WI, T2*-weighted imaging.

Fig. 1A

Fig. 1B

Fig. 1C

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Fig. 1D

R2* map for acute cerebral infarctionA

Y. Shinohara et al. P. 28

B

Y. Shinohara et al. P. 29

C

Y. Shinohara et al. P. 30

D

Y. Shinohara et al. P. 31

Fig. 2. 82-year-old male with CEI in the left MCA territory (patient 6).
DWI demonstrates high signal intensity in the left frontal cortex and insula (A) and MRA reveals occlusion at horizontal segment of left
MCA (B). Corresponding to the occlusion site of MRA, R2* map can show prominent susceptibility effect reflecting fresh thrombus (D,→), while T2*WI shows equivocal findings of the susceptibility effect reflecting thrombus because of the neighboring low signal intensityfrom proximal artery itself (C, ○). CEI, cardiogenic embolic infarction; DWI, diffusion weighted imaging; MCA, middle cerebral artery;
MRA, magnetic resonance angiography; T2*WI, T2*-weighted imaging.

Fig. 2A

A

Fig. 2B

Y. Shinohara et al. P. 32

B

Fig 2D

Fig. 2C

Y. Shinohara et al. P. 33

C

Y. Shinohara et al. P. 34

D

Y. Shinohara et al. P. 35

Fig. 3. 66-year-old male with A-to-A embolism at left terminal ICA (patient 15).
DWI shows high signal intensity in the left occipital cortex (A) and MRA demonstrates left ICA occlusion with decreased in-flow effectof left MCA and left PCA (B). In this case, acute thrombus at left terminal ICA on R2* map (D) is more clearly detected than that on
T2*WI (C), without any apparent susceptibility artifact from the skull base around thrombus. A-to-A, artery-to-artery embolic infarction;
DWI, diffusion weighted imaging; ICA, internal carotid artery; MCA, middle cerebral artery; MRA, magnetic resonance angiography;
PCA, posterior cerebral artery; T2*WI, T2*-weighted imaging.

Fig. 3A

Fig. 3B

Fig. 3C

thrombotic and embolic infarctions clearly.
It has been already known that early recanalization
rate after intravenous rtPA therapy was low in caseswith large proximal arterial occlusions like proximal
middle cerebral artery (MCA) and ICA.13, 21–25 On CT
angiography, clot burden score, which is the scoring
system of the length and location of the thrombus, wasproposed to predict radiological and neurological outcome for thrombolytic therapy or thrombectomy.21–25
Although T2*WI plays an important role for detecting
intra-arterial acute thrombus as susceptibility vessel sign
by reflecting the presence of deoxyhemoglobin within
the clot, susceptibility artifacts from the skull base often disturb the visibility of susceptibility vessel sign at
ICA on T2*WI.10, 13 Therefore, our results showed the207

Fig. 3D

utility of R2* map for detecting thrombus at ICA as well
as MCA indicate a potential of R2* map to be a novel
additional marker predicting the efficacy of intravenous
rt-PA or mechanical thrombectomy.21–25 Furthermore,since therapeutic strategy was different between embolicand atherothrombotic infarctions, we consider that highspecificity of acute thrombus on R2* map also resultsin the selection of optimal therapeutic strategy for acuteischemic stroke.
IDEAL IQ is a commercial software equipped withmulti-echo chemical shift based water-fat separationand simultaneous R2* estimation techniques applying
Dixon method.16–18 Using this software, quantitative ironimage called R2* map, as well as in- and out-of-phase
images, water and fat images and fat fraction map, canY. Shinohara et al.

be obtained by single scanning with short acquisition
time.16–18 The technical aspects of IDEAL IQ, especially the short multi-echo acquisitions, lead to the fact thatR2* map enables to distinguish slight differences of theT2* decay caused by susceptibility effect and visualize
them with reliable image contrast, such as between acutethrombus in ICA and susceptibility artifacts arising fromthe skull base, or peripheral acute thrombus and neighboring intracranial vessels and vessel wall calcifications.
Although IDEAL IQ has been already used forquantitative evaluation of iron deposition and fat fractionof the liver,18 this is the first report that indicates a utility of R2* map by using IDEAL IQ for detecting acutethrombus in the patients with cerebral infarction. We
also performed quantitative evaluation of thrombus andno significant difference was found between CEI and
A-to-A. Cho et al. previously reported that susceptibility
vessels signs on T2*WI were more commonly associated with cardioembolic stroke patients than with otherstroke subtypes including large artery atherosclerosis.8
Liebeskind et al., on the other hand, reported that susceptibility vessel signs on T2*WI reflected histopathology of thrombi: red blood cell-dominant thrombi determined appearance of susceptibility vessel signs, whereas
fibrin-predominant occlusive thrombi determined absence of susceptibility vessel signs.12 However, histopathology of thrombi extracted by endovascular mechanical thrombectomy was unrelated to final determinationof stroke subtypes.12 Therefore, there is not yet a unified
view whether the susceptibility effects of thrombi on
MR imaging enable to determine stroke subtypes or not.
R2* map generated by IDEAL IQ is more sophisticatedquantitative susceptibility-sensitive image than conventional T2*WI. We consider that further examination of
R2* map with larger sample size may lead to clarify its
potential of differentiation between CEI and A-to-A.
Our study has several limitations. First, we used
MRA as reference standard of vessel occlusions in thisstudy. MRA is less accurate as a reference for vessel
occlusion and recanalization than catheter angiographyalthough this modality has proven relatively accurate inevaluating vessel patency.26, 27 Second, we did not consider the difference of signal intensity due to the chronological histopathological change of acute thrombus.
However, it is likely to be less important factor than wethought, as long as the each interval from onset to MR
examination was relatively short like our study. Third,
the sample size was modest especially in the patients of
A-to-A embolism. As mentioned previously, larger sample size will be needed to clarify the efficacy of quantitative evaluation of thrombi on R2* map.
In conclusion, the detectability of fresh thrombus on

R2* map is almost equal to that on T2*WI. Regarding
distal ICA embolism, its detectability on R2* map may
be superior to that on T2*WI. Moreover, R2* map can
provide additional information to differentiate CEI and
A-to-A from ATI.
The authors declare no conflict of interest.

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