Radiol Oncol 2019; 53(4): 427-433. doi: 10.2478/raon-2019-0056
427
research article
Retrieved cerebral thrombi studied by T2 and 
ADC mapping: preliminary results
Jernej Vidmar1,2,3, Franci Bajd4, Zoran V. Milosevic3, Igor J. Kocijancic3, Miran Jeromel3,5, 
Igor Sersa1,2 
1 Institute of Physiology, Medical Faculty, University of Ljubljana, Slovenia
2 Jožef Stefan Institute, Ljubljana, Slovenia
3  Department of Diagnostic and Interventional Neuroradiology, Clinical Institute of Radiology,  
University Medical Centre Ljubljana, Slovenia
4 Faculty of Mathematics and Physics, University of Ljubljana, Slovenia
5 General Hospital Slovenj Gradec, Department of Diagnostic and Interventional Radiology, Slovenia
Radiol Oncol 2019; 53(4): 427-433.
Received 3 October 2019 
Accepted 22 October 2019
Correspondence to: Igor Serša, Ph.D., Jožef Stefan Institute, Jamova cesta 39, SI-2000 Ljubljana, Slovenia, E-mail: igor.sersa@ijs.si
Disclosure: No potential conflicts of interest were disclosed. 
Background. Recent advances in MRI technology makes it increasingly more competitive to CT also in the field of 
interventions. Multi-parametric MRI offers a significant amount of data relevant for characterization of human cerebral 
thrombi.
Patients and methods. Cerebral thrombi of 17 patients diagnosed with acute stroke were acquired by mechanical 
thrombectomy. The thrombi were subsequently scanned using a high spatial-resolution 3D T1-weighted MRI to obtain 
morphological characteristics of the thrombi and also by apparent diffusion coefficient (ADC) and transversal nu-
clear magnetic resonance (NMR) relaxation time (T2) mapping. The MRI results were analysed for possible correlations 
between thrombectomy procedure parameters (recanalization time and number of passes) and MR-measurable 
parameters (sample-mean ADC and T2, within-sample coefficient of variation of ADC and T2, and thrombus length).
Results. Both MRI mapping techniques enabled a good discrimination among thrombi regions of different water 
mobility and compaction. Within-sample coefficient of variation of ADC was found most sensitive for discrimination 
between the thrombi where thrombectomy procedure was performed in a single pass and those where is was per-
formed in two or more passes (p = 0.03). Interestingly, negative correlation was found between the recanalization 
time and thrombus length (ρ = -0.22).
Conclusions. Preliminary results of presented study shows that pretreatment MRI assessment of thrombi in stroke 
patients could potentially ease stroke treatment planning. In this study it is shown that within-sample coefficient of 
variation of ADC could serve for prediction of possible complications during thrombectomy procedures.
Key words: stroke; mechanical thrombectomy; MR microscopy; ADC mapping; T2 mapping
Introduction
Rates of death attributable to cardiovascular dis-
ease have declined, yet the burden of disease re-
mains high.1 The decline is among other factors 
also due to a significant improvement in treatment 
of large vessel occlusions in acute ischemic stroke. 
Early treatment of the stroke is usually based on 
recanalization approaches, namely, administration 
of thrombolytic agents2 and/or mechanical removal 
of thrombi.3 Occluding thrombi may stem from the 
heart or atherosclerotic lesions within or proximal 
to the affected vessel. Histological analysis alone 
is insufficient for determining the origin of occlu-
sive thrombus since both thrombi etiologies, car-
dioembolic and arteriopathic, lead to a formation 
Radiol Oncol 2019; 53(4): 427-433.
Vidmar J et al. / mpMRI of cerebral thrombi428
of thrombi with complex histological patterns that 
overlap.4 MRI was shown to have clinical poten-
tials in thrombi localization and determination of 
its structure and composition.5 Therefore, MRI can 
represent an interesting in vivo alternative to histol-
ogy.
Microscopically, thrombi are composed of plate-
lets and red blood cells (RBCs) interspersed within 
the fibrin meshwork. A fibrin meshwork by itself 
is a permeable porous structure; however, its per-
meability may be strongly influenced by the pres-
ence of platelets as well as of fibrin cross-linking 
which could considerably thicken the meshwork.6,7 
Entrapped RBCs in thrombi8 reduce pore sizes 
within the meshwork and therefore also reduce the 
permeability of the thrombi.9 Furthermore, distri-
bution and proportion of the entrapped blood cells 
in thrombi (RBCs and platelets) influence their 
mechanical properties as well.10 Therefore, overall 
susceptibility of thrombi to thrombolytic treatment 
(thrombolysis or mechanical thrombectomy) is 
strongly influenced by thrombi permeability and 
their mechanical properties.11,12 An accurate assess-
ment of the thrombi structure and composition 
could be helpful in treatment planning and prog-
nosis of recanalization.13,14
Magnetic resonance imaging (MRI) is a sensi-
tive tool for diagnosing ischemic stroke based on 
detecting water mobility in different tissue com-
partments. The detection is enabled by diffusion-
weighted imaging (DWI) followed by a calculation 
of the apparent diffusion constant (ADC) map.15 
Another MRI mapping technique, namely the 
transversal nuclear magnetic resonance (NMR) re-
laxation time (T2) mapping, can be used for char-
acterization of thrombi structure and composition. 
NMR relaxation times are sensitive to molecular 
reorientation or tumbling and are therefore also 
associated with tissue structure and composition.16 
Differences in water mobility and NMR relaxation 
parameters between RBC-rich and platelet-rich 
regions were already found as an efficient dis-
criminating factor for characterization of venous 
thrombi and assessment of their lytic outcome.17 
Specifically, ADC and T2 mapping followed by the 
2D histogram analysis confirmed large structural 
diversity of venous thrombi that differ by their ori-
gin and age.18
The aim of this study is fist to quantitatively 
characterize human cerebral thrombi using multi-
parametric MRI and second to find possible corre-
lations between thrombectomy procedure param-
eters (recanalization time and number of passes) 
and MR-measurable parameters (sample-mean 
ADC and T2, within-sample coefficient of variation 
of ADC and T2, and thrombus length). Preliminary 
results of ongoing research are presented.
Patients and methods
Patients selected for the study (n = 17, mean age = 72 
± 12 years, 10 males and 7 females) were diagnosed 
with acute ischemic stroke due to occluded mid-
dle cerebral artery (MCA; M1 segment). The study 
design followed standard steps of acute ischemic 
stroke management in our tertiary centre. Urgent 
clinical evaluation by a neurologist was followed 
by an urgent multimodal CT imaging (native CT, 
CT perfusion imaging and CT agiography) to con-
firm the diagnosis of an ischemic stroke. The pa-
tients were then treated with the standard full dose 
of rt-PA (0.9 mg/kg, maximum 90 mg) and later, 
due to still presented clinical signs of large cerebral 
artery occlusion, underwent mechanical thrombec-
tomy. All procedures were performed by the same 
skilled interventional neuroradiologist, using the 
same standard mechanical recanalization proce-
dure with the same thrombectomy device (Trevo® 
stent retriever, 4 x 20 mm, Stryker Neurovascular, 
Kalamazoo, MI). For each thrombectomy, the reca-
nalization time was registered as the time between 
the first contact of the thrombectomy device with 
the thrombus and the successful recanalization 
through the occluded artery with complete remov-
al of the thrombus. In addition, for each procedure, 
number of passes with the thrombectomy device 
was registered as well.
The protocol of the study was approved by 
the Institutional Review Board and the Ethical 
Committee of the National Ministry of Health of 
the Republic of Slovenia, approval No. 118/04/14. 
The study was performed in agreement with the 
informed-consent policy.
MR imaging of the retrieved thrombi was per-
formed within 24 hours on an experimental MRI 
scanner consisting of a 2.35 T horizontal-bore 
superconducting magnet (Oxford Instruments, 
Abingdon, United Kingdom) NMR/MRI spectrom-
eter (Tecmag, Houston, TX, USA) and accessories 
for MR microscopy (Bruker, Ettlingen, Germany). 
Each thrombus sample was rinsed with isotonic 
saline of 0.9% w/v of NaCl, pH 7.4 and closed in 
Teflon tubes to prevent tissue desiccation during 
the MR scanning. The tube with the sample was 
then inserted into a 10 mm micro-imaging probe 
and then analyzed by a multi-parametric MRI pro-
tocol consisting of the 3D T1-weighted MRI, fol-
Radiol Oncol 2019; 53(4): 427-433.
Vidmar J et al. / mpMRI of cerebral thrombi 429
lowed by diffusion-weighted imaging (DWI) for 
ADC mapping19 and the multi-spin-echo imaging 
sequence for T2 mapping.20 The imaging param-
eters of the sequences are given in Table 1. During 
MRI scanning, the samples were held at a constant 
room temperature of 22°C.
To obtain five independent MR-measurable pa-
rameters of the thrombi (sample-mean ADC and 
T2 values, their corresponding within-sample co-
efficients of variation CVADC and CVT2 and throm-
bus length) MR images were processed by using 
in-house written image-analysis software that was 
developed within the Matlab programming envi-
ronment (MathWorks, Inc., Natick MA, USA). In 
the MR image processing software, ADC and T2 
values were calculated pixelwise from the masked 
diffusion-weighted and multi-spin-echo images of 
all slices through the entire thrombi volumes by fit-
ting the corresponding exponential functions. For 
each thrombus in the study its sample-mean ADC 
and T2 values and the corresponding within-sam-
ple coefficients of variation CVADC and CVT2 repre-
senting thrombus heterogeneity were calculated 
by analyzing the ADC and T2 maps in all slices 
across the thrombus volume. Similarly, thrombus 
length (Length) of the thrombi were determined 
from the corresponding T1-weighted images as the 
maximum length along the longitudinal direction.
MR-measurable parameters (ADC, T2, CVADC, 
CVT2, Length) of the thrombi in the study were 
then statistically analyzed for their correlations 
with the corresponding recanalization time (RT). 
Possible correlations were studied also between 
length of the thrombi and ADC, T2, CVADC, CVT2. In 
addition, the retrieved thrombi were also classified 
between a group with single pass retrieval, which 
was considered as thrombectomy non-problem-
atic, and a group with multi-pass retrieval where 
the thrombectomy procedure was more difficult to 
perform. The two groups were subsequently sta-
tistically analyzed for significance of differences 
for different MR-measurable parameters using 
Student’s t-test.
Results
Figure 1 depicts T1-weighted images with the cor-
responding ADC and T2 maps of two representa-
tive cerebral thrombi having a different structure 
and morphology. Comparison between ADC 
and T2 maps of both samples in color-coded im-
ages shows a significant variability of ADC values 
across the thrombi for both samples, while their 
T2 maps are more uniform. In ADC maps regions 
with high water mobility (yellow to white regions) 
can be well discriminated from compacted regions 
(blue to violet) where water mobility is much low-
er. T2 maps can still discriminate between regions 
of different compactness/water (serum) content, 
however, not to the same extent.
Figure 2 shows graphs of correlation between the 
recanalization time and different MR-measurable 
thrombi parameters (ADC, T2, CVADC, CVT2, 
Length) as well as with number of passes with the 
thrombectomy device. Similarly, Figure 3 shows 
graphs of correlation between the thrombus length 
and structural and compositional parameters ob-
tained from MR maps (ADC, T2, CVADC, CVT2). In 
TABLE 1. MRI sequence parameters
Sequence parameter
MRI sequence
3D spin-echo 3D PGSE DWI 3D multi-echo
Field of view [mm3] 20 x 10 x 10 20 x 10 x 10 20 x 10 x 10
Imaging matrix 128 x 64 x 64 128 x 64 x 16 128 x 64 x 16
Spatial resolution [μm3] 156 x 156 x 156 156 x 156 x 625 156 x 156 x 625
Echo/inter-echo time [ms] 5 34 16
Repetition time [ms] 100 1035 1930
Signal averages 10 2 2
Number of echoes 1 1 8
b-values [s/mm2] / 0, 260, 620, 1250 /
Scan time [h] 1 4.7 2.3
mpMRI of cerebral thrombi, Figure 1
-9
0
200
0
Sample 1 Sample 2
A
D
C
T 2
T 1
-w
[m2/s]
[ms]
FIGURE 1. Two representative cerebral thrombi presented by central-slice T1-
weighetd images, ADC and T2 maps. Low ADC and T2 values, shown in dark blue, 
correspond to regions of higher compaction while brighter regions are less compact 
regions that are more susceptible to thrombolytic therapy. From the images can also 
be seen that variability of ADC values across the thrombi is considerably higher than 
that of T2 values.
Radiol Oncol 2019; 53(4): 427-433.
Vidmar J et al. / mpMRI of cerebral thrombi430
the graphs, experimental points of different num-
ber of thrombectomy passes are colored differently 
and use different symbols. Correlation between 
different pairs of parameters given by the Pearson 
correlation coefficient is presented in Table 2. From 
the table it can be seen that correlation is the best 
between the recanalization time and the number of 
thrombectomy passes (ρ = 0.92), which is expected. 
Each additional pass in average prolongs the reca-
nalization time for 13 minutes. Other parameters 
do not correlate that well with the recanalization 
time. Among these, correlation was the best with 
CVT2 (ρ = 0.38) and then with thrombus length (ρ 
= -0.22), which is less than expected. Interesting is 
also that thrombus length correlates relatively well 
with ADC (ρ = -0.41).
A closer inspection of correlation graphs in 
Figure 2 shows that distributions are significantly 
different for thrombi retrieved by a single pass 
of the thrombectomy device than for thrombi for 
which retrieval two or more passes were needed. 
In case of the single-pass thrombi group ADC and 
CVADC values are almost uniformly distributed 
over a wider range, while for the thrombi groups 
corresponding to multiple passes the values are 
more localized and are in average shifted to higher 
values for CVADC and to lower values for ADC. This 
observation is confirmed also with the t-test analy-
sis of differences between the single-pass and mul-
ti-pass thrombi groups shown in Table 3. The test 
confirmed significance of difference between the 
groups for parameters ADC (p = 0.05) and CVADC 
(p = 0.03), while for other parameters (T2, CVT2, 
Length) the differences were not found significant.
Discussion
In the study it was shown that MR-measurable 
parameters of a thrombus and parameters of its 
retrieval by mechanical thrombectomy are cor-
related. While no significant correlation was 
found between the recanalization time and MR-
measurable parameters, the parameter coefficient 
of variance of ADC was found efficient for discrim-
ination between thrombi retrieved in a single pass 
of the thrombectomy device and those retrieved by 
multiple passes. This finding is supported by our 
previous observations of thrombi susceptibility to 
thrombolytic treatment.17 In the study ADC was 
found more sensitive to structural and composi-
tional changes in thrombi than T2 and could there-
fore potentially serve for prediction of thrombolyt-
ic treatment outcome. Correlation between the re-
mpMRI of cerebral thrombi, Figure 2
0
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0 1 2 3 4 5 6
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ec
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tim
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[m
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Passes
RT [min]= 13.4 * Passes – 10 
R2 = 0.84 
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ec
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Passes 
1 
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FIGURE 2. Graphs of correlation between the recanalization time (RT) of mechanical 
thrombectomy and different thrombi parameters: sample-mean apparent diffusion 
coefficient (ADC), within-sample coefficient of variation of apparent diffusion 
coefficient (CVADC), sample-mean spin-spin relaxation time (T2), within-sample 
coefficient of variation of spin-spin relaxation time (CVT2), thrombus length (Length), 
and number of thrombectomy procedure passes (Passes). Colour (symbol type) of 
experimental points indicates number of thrombectomy passes.
TABLE 2. Pearson correlation coefficient for different pairs of thrombi parameters. 
Correlation coefficients are sorted by their decreasing absolute values
Pair ρ Pair ρ Pair ρ
Passes-RT 0.92 T2-Passes 0.24 CVADC-Length -0.14
ADC-CVADC -0.43 Length-RT -0.22 Length-Passes -0.13
ADC-Length -0.41 T2-RT 0.21 ADC-T2 0.13
CVT2-RT 0.38 CVADC-Passes 0.19 CVADC-T2 0.12
ADC-CVT2 0.32 CVT2-Length -0.16 ADC-Passes -0.09
CVADC-CVT2 0.28 ADC-RT 0.15 T2-Length 0.06
CVT2-Passes 0.27 CVADC-RT 0.14 T2-CVT2 -0.01
ADC = apparent diffusion coefficient; CVADC = sample coefficient of variation CVADC; CVT2 = sample 
coefficient of variation CVT2; Length = thrombus length; ρ = Pearson correlation coefficient; RT = 
recanalization time 
Radiol Oncol 2019; 53(4): 427-433.
Vidmar J et al. / mpMRI of cerebral thrombi 431
canalization time and thrombus length of ρ = -0.22, 
that was found in the present study, is somewhat 
surprising. Negative correlation between the two 
variables is a surprise, as one would expect that re-
canalization of longer thrombi should take longer21 
and that several passes of the thrombectomy de-
vice are need for retrieval of these. However, in our 
study, the thrombi with the longest recanalization 
time and with most passes of the thrombectomy 
device are of short to medium length (from 5 to 
10 mm). This result indicates a strong influence of 
thrombi composition and compactness on the re-
canalization time. The recanalization time depends 
also on thrombus-vessel wall interactions.22
While thrombus length can be considered as 
a morphological parameter, the other four MR-
measurable parameters are structural-dependent. 
ADC is a direct measure for water mobility in dif-
ferent tissue compartments of thrombi. It decreases 
due to an increased tortuosity and decreased po-
rosity.23 Relaxation time T2 also depends on the 
thrombus microstructure. It is especially sensitive 
to changes in surface-to-volume ratio that when 
increased, can lead to an increased T2 relaxation.16 
Specifically, in Figure 1, low ADC/T2 values can be 
explained by the reduced mobility of water mol-
ecules due to an increased RBC compaction result-
ing in a significant reduction of the extracellular 
space. Another possible mechanism of the ADC/T2 
reduction is a high platelet-to-fibrin content that lo-
cally contracts fibrin meshwork resulting in a pore 
size reduction and extracellular serum expulsion.7 
From Figure 1 it can also be seen that ADC is more 
sensitive to structural changes in thrombi than re-
laxation time T2. ADC maps have higher variability 
than T2 maps, namely, they can better distinguish 
among regions of different compaction/water mo-
bility than T2 maps.
In the study thrombi were sorted into two groups, 
a single- and a multi-pass group, depending on the 
number of thrombectomy device passes performed 
for the retrieval of the thrombus. Classification of 
thrombi between the two groups enabled statistical 
analysis of differences among them using t-test of 
which results are shown in Table 3. The differences 
between the groups were found statistically sig-
nificant (p ≤ 0.05) for parameters CVADC and ADC, 
while they were not significant for CVT2, T2 and 
Length. Lack of significance for these three param-
eters could be due to too small number of samples 
analyzed (n = 17). With more samples included in 
the ongoing study the results of the study would 
be exacter. However, the current number of sam-
ples in the study, though low, was sufficient for 
demonstration of the expected trend between the 
MR-measurable and thrombectomy procedure pa-
TABLE 3. Significance of differences between the single-pass (n = 9) and multi-pass (n = 8) thrombectomy groups for different parameters analysed 
by group-average values and by the t-test
Thrombectomy 
group / t-test
ADC_g 
[10-9 m2/s]
CVADC_g T2_g 
[ms]
CVT2_g Length_g 
[mm]
RT_g 
[min]
Single-pass 0.63 ± 0.1 0.38 ± 0.04 78 ± 10 0.22 ± 0.05 9.3 ± 3.7 4.8 ± 2.8
Multi-pass 0.52 ± 0.1 0.44 ± 0.05 82 ± 11 0.23 ± 0.05 10.4 ± 5.1 27 ± 20
p-value 0.05 0.03 0.41 0.64 0.62 0.006
ADC = apparent diffusion coefficient; ADC_g = group-average of sample-mean ADC; CVADC_g = group-average of within sample coefficient of variation CVADC; CVT2_g = group-
average of within sample coefficient of variation CVT2; Length_g = group-average of thrombus length; p-value = result of the t-test analysis between single- and multi-pass 
thrombectomy groups; RT_g = group-average of recanalization time; T2_g = group-average of sample-mean T2
mpMRI of cerebral thrombi, Figure 3
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FIGURE 3. Graphs of correlation between the thrombus length (Length) and: sample-
mean apparent diffusion coefficient (ADC), within-sample coefficient of variation of 
apparent diffusion coefficient (CVADC), sample-mean spin-spin relaxation time (T2), 
and within-sample coefficient of variation of spin-spin relaxation time (CVT2). Color 
(symbol type) of experimental points indicates number of thrombectomy passes as 
defined in Figure 2.
Radiol Oncol 2019; 53(4): 427-433.
Vidmar J et al. / mpMRI of cerebral thrombi432
rameters. Another limitation of the study was its ex 
vivo design. Because of that some of the measured 
parameters differed from the corresponding values 
in vivo. This is especially true for diffusion-related 
parameters ADC and CVADC. Diffusion is slower 
at room temperature than at body temperature, 
while the relaxation time T2 depends much less on 
temperature. Therefore, it is expected that T2 val-
ues ex vivo are very similar to the corresponding in 
vivo values.24 A special care was also taken to pre-
serve tissue and structural integrity of the retrieved 
thrombi and therefore prevent possible mechanical 
sources for ADC and T2 alternations. This was done 
during the thrombectomy procedure by minimiz-
ing possible thrombi fragmentation and after it by 
preventing tissue desiccation.
Ultimate goal of this research would be to per-
form MRI of thrombi in vivo on patients with acute 
ischemic stroke. Currently, MRI is too slow and 
does not provide sufficient resolution to compete 
with CT. Therefore, this application of MRI is ethi-
cally questionable. However, if thrombi would be 
analyzed in vivo only spectroscopically or imaged 
with very low resolution the scan time would be 
much shorter and information on the sample-mean 
ADC and sample-mean T2 could still be obtained. 
Information on the thrombus length can in princi-
ple be obtained also from high-resolution CT im-
ages. Therefore, practically all the thrombus data 
of this study (apart from CVADC and CVT2) could 
be obtained also in vivo. This information could 
ease decision making in stroke treatment. A proper 
selection of patients eligible for a treatment with 
mechanical recanalization is becoming extremely 
important since the window of thrombectomy for 
ischemic stroke patients was recently extended up 
to 24 hours.25 Therefore, more patients are poten-
tial candidates for the procedure. A possibility of 
the procedure duration time prediction based on 
prior MR imaging of thrombi could significantly 
influence the decision about the thrombectomy in 
selected patients where an extended procedure du-
ration time could present an increased risk of rep-
erfusion related hemorrhage. Information about 
the composition of the thrombus could also in the 
future shift the treatment decision toward mechan-
ical recanalization without pretreatment with the 
thrombolysis (prediction of failed thrombolysis). 
Finally, the information about the thrombus com-
position can also affect the decision making about 
the thrombectomy technique (choosing between 
stent retriever and aspiration device). Preliminary 
data from our study could also have an impact 
on further stent retriever design improvements. 
Namely, the design of the device could be tailored 
to different lengths of thrombi. Short thrombi may 
need a dedicated device, shorter in length but with 
much higher axial force. Alternatively, the aspira-
tion technique may be used as a first modality of 
choice.
Conclusions
Preliminary results of our study shows that MRI 
can provide several parameters that are relevant 
for morphological and structural assessment of 
thrombi. With improvements of MRI technology, it 
can be expected that MRI scanning of patients with 
stroke could complement or even replace standard 
CT scanning in future. Therefore, MR-measurable 
parameters of thrombi, such as those presented in 
this study and perhaps some new ones, could in 
future, in combination with clinical and CT data 
help improving stroke treatment planning and eas-
ing treatment decisions. Results from this ongoing 
study my potentially influence further evolution of 
thrombectomy devices.
Acknowledgment
This study was financially supported by the 
Slovenian Research Agency grant J3-9288.
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