Susceptibility Weighted Imaging: A New Tool in the

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Susceptibility Weighted Imaging: A New Tool in the
Diagnosis of Prostate Cancer and Detection of Prostatic
Calcification
Yan Bai1, Mei-Yun Wang1*., Yan-Hong Han1, She-Wei Dou1, Qing Lin1, Ying Guo1, Wei Li1, DeGang Ding2, Jian-Ping Dai1, Wei Qin5, Da-Peng Shi1*., Jie Tian4*., Yong-Ming Dai3
1 Department of Radiology, Henan Provincial People’s Hospital, Zhengzhou, Henan, China, 2 Department of Urinary Surgery, Henan Provincial People’s Hospital,
Zhengzhou, Henan, China, 3 MRI, Siemens Healthcare, Shanghai, China, 4 Institute of Automation, Chinese Academy of Sciences, Beijing, China, 5 Life Science Research
Center, School of Sciences and Technology, Xidian University, Xi’an, Shanxi, China
Abstract
Background: Susceptibility weighted imaging (SWI) is a new MRI technique which has been proved very useful in the
diagnosis of brain diseases, but few study was performed on its value in prostatic diseases. The aim of the present study was
to investigate the value of SWI in distinguishing prostate cancer from benign prostatic hyperplasia and detecting prostatic
calcification.
Methodology/Principal Findings: 23 patients with prostate cancer and 53 patients with benign prostatic hyperplasia
proved by prostate biopsy were scanned on a 3.0T MR and a 16-row CT scanner. High-resolution SWI, conventional MRI and
CT were performed on all patients. The MRI and CT findings, especially SWI, were analyzed and compared. The analyses
revealed that 19 out of 23 patients with prostate cancer presented hemorrhage within tumor area on SWI. However, in 53
patients with benign prostatic hyperplasia, hemorrhage was detected only in 1 patient in prostate by SWI. When comparing
SWI, conventional MRI and CT in detecting prostate cancer hemorrhage, out of the 19 patients with prostate cancer who
had prostatic hemorrhage detected by SWI, the prostatic hemorrhage was detected in only 7 patients by using conventional
MRI, and none was detected by CT. In addition, CT demonstrated calcifications in 22 patients which were all detected by SWI
whereas only 3 were detected by conventional MRI. Compared to CT, SWI showed 100% in the diagnostic sensitivity,
specificity, accuracy, positive predictive value(PPV) and negative predictive value(NPV) in detecting calcifications in prostate
but conventional MRI demonstrated 13.6% in sensitivity, 100% in specificity, 75% in accuracy, 100% in PPV and 74% in NPV.
Conclusions: More apparent prostate hemorrhages were detected on SWI than on conventional MRI or CT. SWI may provide
valuable information for the differential diagnosis between prostate cancer and prostatic hyperplasia. Filtered phase images
can identify prostatic calcifications as well as CT.
Citation: Bai Y, Wang M-Y, Han Y-H, Dou S-W, Lin Q, et al. (2013) Susceptibility Weighted Imaging: A New Tool in the Diagnosis of Prostate Cancer and Detection
of Prostatic Calcification. PLoS ONE 8(1): e53237. doi:10.1371/journal.pone.0053237
Editor: Xiaoliang Zhang, University of California San Francisco, United States of America
Received June 25, 2012; Accepted November 27, 2012; Published January 7, 2013
Copyright: ß 2013 Bai et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by the National Natural Science Foundation of China under Grant Nos. 81271565, the Distinguished Young Scholar in
Scientific and Technical Innovation Foundation of Henan Province under Grant No.124100510016, and the Science and Technology Foundation of Public Health of
Henan Province under Grant Nos.201202018 and 201003095. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: Author (Yong-Ming Dai) from a commercial company, Siemens Healthcare, was a MR collaboration manager doing technique support in
this study under Siemens collaboration regulation without any payment and personal concern regarding with this study. This does not alter the authors’
adherence to all the PLOS ONE policies on sharing data and materials.
* E-mail: [email protected] (MYW); [email protected] (DPS); [email protected] (JT)
. These authors contributed equally to this work.
intensity (SI) of calcification is varied [3,4] and the size of
calcification is usually very small.
Susceptibility weighted imaging (SWI) is a new MRI technology
which reflects the magnetic susceptibility of tissue and is exquisitely
sensitive to paramagnetic deoxygenated blood products such as
deoxyhemoglobin, methemoglobin and haemosiderin [5]. It
includes not only magnitude information but also useful phase
information, which was usually ignored in most diagnostic MR
imaging. To make good use of phase information, though phase
and magnitude images separately are also critical pieces of
information, Dr. Haacke et al. combined the filtered phase and
Introduction
Prostate cancer is the fifth most common cancer [1] and
become a major worldwide public health problem [2], which
causes 6% of cancer deaths in men [1]. MRI has been a useful tool
to detect PCa, but it’s still difficult to distinguish Prostate cancer
from benign prostatic hyperplasia sometimes, especially when the
tumor is located in the central zone of prostate. In addition,
prostatic calcification is also difficult to be detected clearly by
conventional magnetic resonance imaging (MRI) as the signal
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Susceptibility Weighted Imaging in Prostate Cancer
the magnitude information and thus created a new susceptibilityweighted magnitude image, i.e. SWI [6]. SWI was proved to be
much more sensitive in detecting microbleeds in brain thangradient-recalled echo (GRE)- and GRE-type single-shot echoplanar
imaging (GREI, GRE-EPI) [7]. Because diamagnetic calcification
and paramagnetic blood products present opposite signal features
on the filtered phase images, it is easy to distinguish calcification
from hemorrhage by using filtered phase image [8]. Thus SWI
and filtered phase image has been widely used in the detection of
intracerebral microbleed and display of calcification in central
nervous system [9–12]. However, there are no reports on SWI in
prostate so far. This study investigated the value of high-resolution
SWI and filtered phase image in distinguishing prostate cancer
from benign prostatic hyperplasia and detecting calcification by
comparing with conventional MR and CT images.
Table 1. Characteristics of 23 male patients with prostate
cancer.
Case No./age (year)
SWI
Location of Pca
1/79
Hemorrhage
Central Zone
2/78
Hemorrhage
Peripheral Zone
3/68
Hemorrhage
Central Zone
4/91
Hemorrhage
Peripheral Zone
5/78
Hemorrhage
Peripheral Zone
6/64
Hemorrhage
Peripheral Zone
7/55
Hemorrhage
Central Zone
8/72
Hemorrhage
Peripheral Zone
9/76
Hemorrhage
Peripheral Zone
Materials and Methods
10/79
Hemorrhage
Peripheral Zone
Ethics Statement
11/70
Hemorrhage
Peripheral Zone
This study was approved by the hospital review boards of
Henan Provincial People’s Hospital. Written informed consent
was obtained from all patients. All research procedures were
conducted in accordance with the Declaration of Helsinki.
12/71
Hemorrhage
Peripheral Zone
13/70
Hemorrhage
Peripheral Zone
14/56
Hemorrhage
Peripheral Zone
15/68
Hemorrhage
Peripheral Zone
16/73
Negative
Peripheral Zone
17/76
Negative
Peripheral Zone
18/71
Negative
Peripheral Zone
19/66
Hemorrhage
Peripheral Zone
20/72
Hemorrhage
Peripheral Zone
Study Population
This was a prospective study enrolling 76 patients with prostate
diseases in Henan Provincial People’s Hospital from June 2011 to
September 2012. Transrectal ultrasonography (TRUS)-guided
prostate biopsy proved 23 patients with prostate cancer (age range
55–91 years, average age 71 years) (Table 1) and 53 patients with
benign prostatic hyperplasia (age range 49–84 years, average age
68 years). High-resolution SWI, conventional MRI and CT were
performed on all patients prior to prostate biopsy, transurethral
resection, endocrine therapy, brachytherapy, radiotherapy or drug
treatment for the prostate disease.
Imaging acquisition. MRI was performed on a Siemens 3T
scanner (Magnetom Trio, Siemens Medical Solutions, Erlangen,
Germany) with a pelvic array phased coil (Siemens Medical
System).
SWI is a three-dimensional fast low-angle gradient-echo (GRE)
sequence. The imaging parameters of SWI for prostate are as
follows: field of view (FOV) 3006300 mm2, matrix 2826512, TR
(repetition time)/TE (echo time) = 22/12 milliseconds (ms), 20u
flip angle, and 3 mm slice thickness. The acquisition time was 3
minutes and 36 seconds. The SWI images were created by using
the magnitude and phase images [13]. The phase image was high
pass filtered (by using a 64664 exclusion of low-spatial-frequency
information) to remove much of the spine’s low spatial frequency
background static field variation. A phase mask was created by
setting all positive phase values (between 0u and 180u) to unity and
normalizing the negative-phase values ranging from 0u to 2180u
to a gray scale of values ranging linearly from 1 to 0, respectively.
This normalized phase mask was multiplied four times against the
original magnitude image and yielded images that maximized the
negative signal intensities of the regions containing deoxygenated
blood and increased the contrast between regions containing
deoxygenated blood and the surrounding tissue. Finally, a minimum intensity projection over two sections was performed to
display the processed data by using contiguous 4-mm-thick
sections in the transverse plane.
Conventional MRI was performed with a fast spin-echo (FSE)
sequence. The imaging parameters were as follows:
Axial T1- weighted image (WI): field of view (FOV)
3006300 mm2, matrix 2886320, TR (repetition time)/TE (echo
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21/60
Hemorrhage
Peripheral Zone
22/71
Negative
Central Zone
23/69
Hemorrhage
Peripheral Zone
doi:10.1371/journal.pone.0053237.t001
time) = 700/11 milliseconds (ms), 150u flip angle, and 3 mm slice
thickness. The acquisition time was 3 minutes and 25 seconds.
Axial T2WI: FOV 3006300 mm2, matrix 2726320, TR/
TE = 4000/87 ms, 140u flip angle, and 3 mm slice thickness. The
acquisition time was 3 minutes and 54 seconds.
Sagittal T2WI: FOV 2506250 mm2, matrix 2726320, TR/
TE = 4000/87 ms, 140u flip angle, and 3 mm slice thickness. The
acquisition time was 3 minutes and 54 seconds.
Coronal T2WI: FOV 2506250 mm2, matrix 1926256, TR/
TE = 4000/104 ms, 145u flip angle, and 4 mm slice thickness. The
acquisition time was 2 minutes and 26 seconds.
CT was performed on a 16-row CT scanner (Brilliance 16,
Philips Medical Systems). The imaging parameters are as follows:
120KV tube voltage, 250 mA tube current, and 3 mm thickness.
Histopathologic examination. Each patient underwent
transrectal ultrasound-guided sextant biopsies after completion of
the MRI and CT examination within 10 days. The pathological
results revealed that 23 patients had prostate cancer and 53
patients had benign prostatic hyperplasia.
Imaging analysis. Two radiologists with 11 and 15 years’
diagnostic experience, respectively, blinded to the histopathologic
results analyzed all images. Tumorous and non-neoplastic areas
were determined on the MR images in patients with prostate
cancer. They observed the hemorrhagic foci and calcification in
the prostate and discussed the final results when disaccordance
appeared.
Statistical analysis. SPSS 17.0 statistical software was used
to analyze data. Fisher’s exact test was used to analyze the
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Susceptibility Weighted Imaging in Prostate Cancer
were located in the central zone of the prostate in this study, and
tumor hemorrhage were detected in 3 patients by SWI.
The calcificatinos were detected in 22 patients by CT, including
5 out of 23 patients with prostate cancer and 17 out of 53 patients
with benign prostatic hyperplasia.When MRIs were used, the
calcifications were detected in all the 22 patients by SWI whereas
in only 3 by routine MRI (Fig. 3, 4). Compared to CT, SWI
showed 100% in the diagnostic sensitivity, specificity, accuracy,
positive predictive value and negative predictive value in detecting
calcifications in prostate but conventional MRI demonstrated
13.6% in diagnostic sensitivity, 100% in specificity, 75% in
accuracy, 100% in positive predictive value and 74% in negative
predictive value.
hemorrhagic manifestations on SWI between prostate cancer and
benign prostatic hyperplasia group. A p value of less than 0.05 was
considered significant. The sensitivity, specificity, accuracy,
negative predictive values (NPV) and positive predictive values
(PPV) at SWI and conventional MRI in detecting calcifications in
prostate were evaluated using CT as the gold standard.
Results
The tumor lesions of 19 patients with prostate cancer were
located in the peripheral zone of the prostate, only 4 cases were
within the central region. In 19 out of 23 patients (82.6%) with
prostate cancer, hemorrhage was detected within the tumorous
areas (16 patients with prostate cancer in the peripheral zone and
3 patients with tumor lesions in the central zone) by SWI (Table 1).
However, small hemorrhage was detected only in 1 patient out of
53 (1.9%) patients with benign prostatic hyperplasia. Fisher’s exact
test showed significant difference between prostate cancer and
benign prostatic hyperplasia in the detection of hemorrhage within
lesions (P,0.05). Out of the 19 patients with prostate cancer who
had prostatic hemorrhage detected by SWI, only 7 patients had
prostatic hemorrhage on conventional MRI (Figs. 1, 2, 3).
Bleeding was not detected in all the patients by using CT. More
importantly, the tumor lesions of 4 patients with prostate cancer
Discussion
SWI is a new MRI technique which is more sensitive than CT,
conventional MR and T2*WI GRE sequences in detecting
paramagnetic blood products such as deoxyhemoglobin, methemoglobin and haemosiderin in central nervous system [5]. It has
been widely used in detecting microbleeds in a variety of brain
diseases such as brain trauma, stroke and vascular malformation
[8–11]. In addition, SWI in spinal cord trauma has also been
investigated by our team and was proved valuable in detecting
spinal cord hemorrhage [14]. Some recent studies in glioma have
Figure 1. A 64-year-old man with prostate cancer in peripheral zone of the prostate. Heterogeneous signal on conventional T1WI (A) and
T2WI (B) (arrows) indicates tumor hemorrhage. No hemorrhage is demonstrated on CT (C). The tumor hemorrhage was also seen with SWI (D) and
filtered phase image (E) (arrows). Histopathologic examination confirmed the diagnosis of prostate cancer (F).
doi:10.1371/journal.pone.0053237.g001
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Figure 2. A 55-year-old man with prostate cancer in central zone of the prostate. No tumor hemorrhage is demonstrated on conventional
T1WI (A), T2WI (B) and CT (C), but low signal within tumor on SWI (D) and filtered phase image (E) (arrows) indicates tumor hemorrhage.
Histopathologic examination confirmed the diagnosis of prostate cancer (F).
doi:10.1371/journal.pone.0053237.g002
Figure 3. A 66-year-old man with prostate cancer in peripheral zone of the prostate. Low signal on conventional T1WI (A) and T2WI (B)
(arrows) indicates tumor hemorrhage. No hemorrhage is demonstrated on CT (C). The tumor hemorrhage was also seen with SWI (D) and filtered
phase image (E) (arrows). The images in second row come from another slice of the same patient. No prostatic calcification is demonstrated on
conventional T1WI (F) and T2WI (G), but dot-like high density on CT (H), low signal on SWI (I) and high signal on filtered phase image (J) (arrows)
indicates calcificaiton.
doi:10.1371/journal.pone.0053237.g003
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Figure 4. A 62-year-old man with benign prostatic hyperplasia. No prostatic calcification is demonstrated on conventional T1WI (A) and T2WI
(B), but dot-like high density on CT (C), low signal on SWI (D) and high signal on filtered phase image (E) (arrows) indicates calcificaiton.
doi:10.1371/journal.pone.0053237.g004
with prostate cancer, hemorrhage was detected in 19 patients
within the tumorous areas by SWI (82.6%). However, small
hemorrhage was detected only in 1 patient out of 53 (1.9%)
patients with benign prostatic hyperplasia by SWI. The hemorrhage ratio within the lesions had significant difference between
the two diseases. From this result, it seemed that prostate cancer
may be more prone to bleeding than benign prostatic hyperplasia.
The possible reason may be that the prostate cancer tissue has
higher microvessel density (MVD) which was caused by increased
vascular endothelial growth factor (VEGF) expression than normal
prostate or benign prostatic hyperplasia tissue [21,22]. Overexpression of Id-1 (inhibitor of differentiation/DNA synthesis)
which belongs to the Id family of helix–loop–helix proteins is a key
factor in promoting angiogenesis through activation of the VEGF
in prostate cancer cells [23]. The new microvessels in tumors
generally differ from those of noncancerous tissue. Although
tumorous area contains a greater number of vessels than nonneoplastic area, the vessel surface area density is reduced. This
reflected that the size and shape of tumor microvessels tend to be
broad and less branched than those in normal tissue [24]. It may
lead to bleeding in prostate cancer as the new microvessels are
more fragile and irregular with increased permeability and higher
proliferation rate than that of normal endothelial cells [21]. Blood
ow measured in tumor-containing prostate is generally higher than
that in prostates tissue containing benign prostatic hyperplasia
[25]. The differences between prostate cancer and benign prostatic
explored SWI’s value and found that it’s helpful in tumor grading
and patient management strategies [15,16]. But so far no studies
have been done on the value of SWI in prostate cancer and other
prostate diseases.
As an advanced imaging technique, MRI has been gaining
acceptance as an important tool in the evaluation of prostate
diseases. T2WI is an important traditional sequence for the
diagnosis of prostate cancer in the prostate peripheral zone but not
specific. It is easy to distinguish the cancerous area which presents
hypointense on T2WI from the uniform hyperintense background
in the prostate peripheral zone. However, other changes such as
prostatitis and fibrosis also can appear hypointense on T2WI [17].
Furthermore, although most of cancers arise in the peripheral
zone of the prostate, up to 30% of prostate cancers occur within
the central region [18]. It is more difficult to discriminate
malignant from benign prostatic hyperplasia because transition
zone cancer is the site of origin of benign prostatic hyperplasia,
which can have a heterogeneous appearance [19]. Although
diffusion weighted imaging (DWI), magnetic resonance spectroscopy (MRS) and dynamic contrast enhanced (DCE) imaging may
provide supplementary information for the diagnosis of prostate
disease, as each method has its own deficiencies, overlap appears
in the differential diagnosis between prostatic cancer and benign
prostatic hyperplasia [20].
This study investigated the potential of SWI in distinguishing
prostate cancer from benign prostatic hyperplasia. In 23 patients
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Susceptibility Weighted Imaging in Prostate Cancer
hyperplasia in microvascular structure and hemodynamics may be
the main reasons of high incidence of prostate cancer bleeding. In
addition, out of the 19 patients with prostate cancer who had
prostatic hemorrhage detected by SWI in this study, conventional
MRI only detected prostatic hemorrhage in 7 patients. It
suggested that SWI is more sensitive in detecting prostatic
hemorrhage than conventional MRI. More importantly, the
tumor lesions of three patients with prostate cancer were located
in the central zone of the prostate in this study, and tumor
hemorrhage were all detected in these three patients by SWI. This
finding would be very helpful for the accurate diagnosis of prostate
cancer in central zone. Although not all patients with prostate
cancer demonstrated hemorrhage on SWI, the supplementary
information provided by SWI may be valuable for the diagnosis of
prostate cancer. As the sample size of this study was small, more
larger studies need to be performed to further prove these results.
Prostatic calcification is frequently encountered in urological
practice. Some reports revealed that small, multiple calcifications
are a normal, often incidental ultrasonographic finding in the
prostate and represent a result of age rather than a pathologic
entity. However, larger prostatic calcification may be related to
underlying inflammation and require further evaluation and
possible treatment [26,27]. Traditionally, CT is thought the gold
standard for detection of calcification which can be determined
with Hounsfield units (Hu) above 100 [28]. On routine MRI, the
signal of calcification is varied because of diverse calcium
compounds and difficult to distinguish it from hemorrhage.
Therefore, the ability of CT in detecting calcification is far greater
than conventional MRI. With the development of MRI techniques, filtered phase image has become a very sensitive technique
in detecting calcification in brain [8], but no study was performed
to investigate its value in detecting prostatic calcification. This
study demonstrated that filtered phase image has equal efficiency
in detecting prostatic calcification as CT and far higher efficiency
than routine MRI. The mechanism may be that filtered phase
image is exquisitely sensitive to differences in local magnetic
susceptibility, which can be induced by both hemorrhage and
calcification [5]. Both calcification and hemorrhage show low
signal on SWI, but present opposite signal features on filtered
phase images. Usually calcification is high signal or mixed signal
dominated by high signal but hemorrhage displays as low signal or
mixed signal dominated by low signal on filtered phase images
[29]. So filtered phase image is useful in distinguishing calcification
from hemorrhage. To overcome ill-posed nature of the inverse
filter and improve susceptibility quantification, Dr. Haacke et al.
introduced a form of susceptibility mapping to produce an image
of veins from phase data [30]. Both simulations and human studies
have demonstrated that this approach can dramatically reduce
streaking artifacts and improve the accuracy of susceptibility
quantification inside the structures of interest such as veins or
other brain tissues [31]. In the future, it may be possible to use this
approach to evaluate quantitatively microbleeds and calcifications
and allow a straightforward identification of calcification.
The major limitation of this study is that the histopathologic
examination were all performed by biopsy instead of prostate
resection. So the tumor hemorrhage on SWI was not directly
proved by histopathologic examinations. In addition, the sample
size in this study is not very large so we did not evaluate the
incidence of tumor bleeding at different stages in patients with
prostate cancer. Future studies may need to get more reliable
results and investigate the potential of SWI in the prostate cancer
staging.
In conclusion, our results indicate that SWI is more sensitive in
the detection of prostate microbleeding and may be helpful in the
differential diagnosis between prostatic cancer and benign
prostatic hyperplasia. Filtered phase images can identify prostate
calcifications as well as CT. More studies with larger sample size
are needed to get more reliable results for clinical practice in the
future.
Acknowledgments
We wish to thank Dr. E. Mark Haacke in deparment of Radiology in
Wayne State University in USA for manuscript review.
Author Contributions
Guarantor of integrity of the entire study: MYW YB DGD DPS. Study
concepts: MYW YB DPS. Definition of intellectual content: MYW YB
YHH DPS. Literature research: MYW YB YHH DGD JPD DPS YMD.
Clinical studies: MYW YB YHH SWD QL YG WL DGD DPS. Statistical
analysis: MYW YB DPS JT WQ. Manuscript editing: MYW YB DGD
JPD DPS YMD JT WQ. Manuscript review: MYW YB YHH SWD QL
YG WL DGD JPD DPS YMD. Conceived and designed the experiments:
MYW YB YHH DGD DPS. Performed the experiments: YB YHH MYW
SWD QL YG WL DGD. Analyzed the data: MYW YB YHH DGD DPS
YMD JT WQ. Contributed reagents/materials/analysis tools: YB YHH
SWD QL YG WL. Wrote the paper: YB MYW.
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PLOS ONE | www.plosone.org
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January 2013 | Volume 8 | Issue 1 | e53237

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