T2-weighted MR imaging of prostate cancer: multishot echo-planar imaging vs fast

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Eur Radiol (2004) 14:318–325
DOI 10.1007/s00330-003-2118-y
Tsutomu Tamada
Teruki Sone
Kiyohisa Nagai
Yoshimasa Jo
Masayuki Gyoten
Shigeki Imai
Yasumasa Kajihara
Masao Fukunaga
Received: 31 December 2002
Revised: 22 May 2002
Accepted: 15 September 2003
Published online: 18 October 2003
© Springer-Verlag 2003
T. Tamada (✉) · T. Sone · K. Nagai
M. Gyoten · S. Imai · Y. Kajihara
M. Fukunaga
Department of Radiology,
Kawasaki Medical School,
577 Matsushima, 701-0192 Kurashiki City,
Okayama, Japan
e-mail: [email protected]
Tel.: +81-86-4621111
Fax: +81-86-4621199
Y. Jo
Department of Urology,
Kawasaki Medical School,
577 Matsushima, 701-0192 Kurashiki City,
Okayama, Japan
U R O G E N I TA L
T2-weighted MR imaging of prostate cancer:
multishot echo-planar imaging vs fast
spin-echo imaging
Abstract The aim of the present
study was to assess the performance
of pre-biopsy T2-weighted MR imaging using multishot echo-planar
imaging (EPI) sequence for visualization of prostate cancer and to
compare image quality with that of
fast spin-echo (FSE) sequence. Thirty-nine patients with suspected prostate cancer and one healthy male
volunteer were examined on a 1.5-T
MR scanner equipped with a pelvic
phased-array coil. Axial MR images
were obtained using multishot EPI
sequence with a multishot number
of 16 and FSE sequence without fat
suppression. Paired EPI and FSE
images were independently evaluated by three radiologists. Furthermore, signal-to-noise ratio (SNR)
and contrast-to-noise ratio (CNR)
were compared between EPI and
FSE images of 12 pathologically
proven lesions of prostate cancer.
Delineation of the periprostatic venous plexus, prostate zonal anatomy,
Introduction
The incidence of prostate cancer is high in Caucasians
and the mortality rate from prostate cancer is higher
than that from lung cancer and colorectal cancer in
males aged 65 years or more in the United States [1].
The incidence of prostate cancer in Japanese has
been several-fold lower than that in Caucasians but is
likely to increase with recent westernization of life
style and with the increase in the number of the aged
[2, 3].
and seminal vesicle on EPI was
graded to be superior/inferior to FSE
in 15.8/0, 14.6/0, and 21.5/4.3% of
cases, respectively. On the other
hand, delineation of the neurovascular bundle was superior/inferior to
FSE in 2.6/13.2% of cases. The
SNR and CNR of prostate cancer on
EPI were significantly higher than
those on FSE (7.99±2.51 vs
3.36±0.58, p<0.0001, and 5.51±2.02
vs 2.21±0.79, p<0.0001, respectively). In conclusion, multishot EPI has
higher quality of contrast resolution
for imaging of prostate cancer compared with FSE and would have the
potential usefulness in the detection
of prostate cancer, although these results obtained with a phased-array
coil cannot be extrapolated to examinations performed with an endorectal coil.
Keywords Prostate · Neoplasms ·
MR imaging · Echo-planar imaging ·
Comparative studies
Magnetic resonance imaging is used for detection of
the location and extracapsular spread of tumor in prostate cancer, and its usefulness is being established [4].
In MR imaging, T2-weighted images using fast spinecho (FSE) sequence are generally used for an evaluation of the internal structure of the prostate [5, 6]. The
most cancer nodules arise in the peripheral zone and are
of low signal intensity compared with an inherently
high signal intensity of the peripheral zone by this
method. Since 512 matrix can be used in T2-weighted
FSE imaging either with body coil or endorectal surface
319
coil, high spatial resolution is obtained with a short acquisition time; however, the limitation of conventional
or FSE imaging also exists and 30–40% of prostate
cancer in the peripheral zone are undetectable because
the lesions are isointense to the peripheral zone [7, 8, 9,
10].
Echo-planar imaging (EPI) with high temporal
and contrast resolution developed by Mansfield [11] is
used in diffusion-weighted imaging of acute stroke
[12], perfusion imaging [13], and functional imaging
[14]. In the imaging of prostate lesions, however, the
usefulness of EPI sequence has not been thoroughly
evaluated. In the present study, we focused on high
contrast resolution rather than high temporal resolution
in EPI, applied the EPI sequence to the imaging of the
prostate, and assessed its usefulness in the delineation
of prostate normal structures and the detectability of the
prostate cancer as compared with T2-weighted FSE imaging.
Subjects and methods
Patient characteristics
Thirty-nine male patients (age range 53–84 years, mean age
71 years) with suspected prostate cancer were referred for MR imaging of the pelvis between October 1997 and April 1998. One
healthy male volunteer 29 years old also underwent MR examination for selection of the imaging parameters on multishot EPI. The
inclusion criteria of the patients were based on a positive digital
rectal examination and/or high prostate-specific antigen (PSA)
levels, and a transrectal ultrasound (TRUS)-guided biopsy of the
prostate performed after MR imaging. Informed consent was obtained from all participants after the nature of the procedures had
been fully explained.
MR imaging
The MR images were obtained with a 1.5-T whole-body imager
(Signa Horizon, General Electric, Milwaukee, Wis.). The pelvic
phased-array coil (Pelvic Array, General Electric) was used as a
receive-only surface coil. After intramuscular administration of
glucagon to decrease intestinal peristalsis, imaging was performed
in all patients under fasting. After a localized series of coronal T1weighted images were obtained, axial and sagittal T2-weighted
FSE sequence, axial EPI sequence, and other routine sequences
were performed sequentially. The examination was generally completed in 40–50 min. Axial sections were obtained with 4- to 5mm slice thickness and 0- to 1-mm interslice gap and a 24-cm
field of view. T2-weighted FSE images were obtained using a TR
time of 4000 ms, an effective TE time of 110 ms, an echo train
length of 9 or 10, a receiver band width of 15.6 kHz, two or three
averagings, a 512¥320 acquisition matrix, and no fat-suppression
technique.
The T2-weighted EPI parameters were examined in the healthy
subject. In EPI, the spin-echo type, which has been reported to be
less sensitive to the magnetic susceptibility and blood flow artifacts [11], was used. As EPI parameters, the multishot number, effective TE, and the receiver bandwidth were examined. The optimal parameters obtained from the study were used for EPI of the
remaining subjects. The imaging time was 5 min 23 s in EPI, and
between 4 min 48 s and 6 min 24 s in FSE.
Image interpretation and data analysis
Paired axial images of T2-weighted EPI and FSE sequences were
evaluated. Three radiologists independently compared EPI and
FSE images in terms of delineation of normal structures, i.e., the
periprostatic venous plexus in 40 subjects, the prostate zonal anatomy in 32 subjects, the neurovascular bundle in 38 subjects, and
the seminal vesicle in 31 subjects, and judged using a relative
three-point scale to determine whether the EPI images were better
than, the same as, or worse than the FSE images. The prostate
zonal anatomy in 8 patients, the neurovascular bundle in 2 patients, and the seminal vesicle in 9 patients were excluded for the
evaluation because normal structure was disappeared due to the
tumor invasion or hemorrhage. The pooled results of three reviewers were used to compare the ratings in the two sequences. The
statistical analyses were performed using the paired sign test with
a value of p<0.05 considered significant.
Twenty-seven patients were pathologically confirmed prostate
cancer by transrectal needle biopsy. The biopsy specimen was obtained from each sextant under the guidance of TRUS. An additional biopsy was taken when necessary from the area as close as
possible to the suspected region on MR images. All biopsy specimens were evaluated by a pathologist in our hospital. Of the 27
patients, 15 patients with tumor in the inner gland, hemorrhage in
the prostate, or disappearance of the normal peripheral zone
caused by tumor invasion were excluded, and signal-to-noise ratio
(SNR) of the tumor and contrast-to-noise ratio of the tumor [CNR;
(SI of the peripheral zone as the control-SI of lesion) noise] of
EPI and FSE T2-weighted images were calculated. On MR images, the lesion fulfilling the following criteria was regarded to be
the prostate cancer: an area in the posterior aspect of the peripheral zone with (a) diffuse low SI with mass effect, or (b) circumscribed, round, or triangular-shaped localized hypointensity in
comparison with the normally hyperintense appearance of the peripheral zone, and (c) a size larger than 5 mm. Locations of all the
suspected lesions on MR images were consistent with the estimation by TRUS-guided needle biopsy. All 12 patients had adenocarcinoma, and pathologically Gleason score was 2 in 2 patients, 3 in
1 patient, 5 in 5 patients, 7 in 2 patients, 8 in 1 patient, and 9 in 1
patient. Only one lesion per patient was analyzed. The region of
interest (ROI) for the SI measurements was established in the largest possible area to lesion and in the same site for each sequence
(Fig. 1). In the peripheral zone, 5 ROIs were placed in the normal
area excluding the lesion, and 5 ROIs were placed at arbitrary positions in the areas of anterior and posterior across the pelvis
which for the noise measurements. Their means were used for the
determination of the SNR and CNR. Calculated SNR and CNR
values of each sequence were expressed as the means±SD, and
compared using Student’s t test. The results were considered significant at p<0.05.
Results
Evaluation of T2-weighted EPI parameters
The EPI images obtained from healthy subject using 1,
2, 4, 8, 16, or 32 shots, an effective TE time of 40, 60,
80, 100, and 120 ms, and a receiver band width of 16,
32, and 64 kHz were evaluated. The images obtained using 16 and 32 shots had less distortion (Fig. 2). The images with high contrast resolution of prostate zonal anatomy were obtained using an effective TE of 80 ms
(Fig. 3), and images with fewer artifacts were obtained
using a receiver bandwidth of 64 kHz (Fig. 4). Based on
320
Fig. 1 Example of the placement of region of interest
(ROI) for signal intensity (SI)
measurements in a axial multishot echo-planar image and
b fast spin-echo image for the
patient with pT3 prostate cancer. Both images show low SI
lesion in the left peripheral
zone. ROI 1 and ROI 2–6 are
the regions for the SI measurement of lesion and control area
in the peripheral zone, respectively. S/N SI of lesion/noise,
C/N [(SI of the peripheral zone
(the average of SI in ROI
2–6)-SI of lesion)/noise]
Fig. 2a–f A 29-year-old healthy man. Axial sections by
echo-planar imaging with the
shot number of a 1, b 2, c 4,
d 8, e 16, and f 32. With four
averagings and an effective TE
time of 80 ms, acquisition
times were a 20 s, b 45 s,
c 1 min 25 s, d 1 min 23 s,
e 2 min 43 s, and f 5 min 23 s.
Image matrix size was 256¥128
in single-shot images and
256¥256 in multishot images
these results, 16 shots, TR time of 2499 ms, an effective
TE time of 80 ms, a receiver band width of 62 kHz, eight
averagings, and a 256¥256 acquisition matrix on EPI sequence were the optimal conditions to obtain images using the same sections and almost the same acquisition
time as T2-weighted FSE imaging.
Comparison between EPI and FSE images in delineating
normal anatomy
The ratings of the delineation for normal anatomy are
shown in Table 1. According to the judgment of the delineation of the normal anatomy performed by individual
three radiologists, the periprostatic venous plexus, prostate zonal anatomy, and seminal vesicle on EPI sequence
was rated superior to that on FSE sequence in 19
321
Fig. 3a–e A 29-year-old healthy man. Axial sections by
multishot echo-planar imaging
with the multishot number of
16, and four averagings. The
effective TE times were a 40,
b 60, c 80, d 100, and e 120 ms
Fig. 4a–c A 29-year-old healthy man. Axial sections by
multishot echo-planar imaging
with the multishot number of
16, effective TE time of 80 ms,
and four averagings. The receiver bandwidth was a 16,
b 32, and c 64 kHz
(15.8%) of 120 cases, 14 (14.6%) of 96 cases, and 20
(21.5%) of 93 cases, respectively, whereas EPI images
was judged to inferior to that on FSE images only in 4
(4.3%) of the 93 cases in the seminal vesicle (Figs. 5, 6).
On the other hand, neurovascular bundle on EPI images
was rated inferior to that on FSE images in 15 (13.2%)
of 114 cases, and superior to that in only 3 cases (2.6%).
Comparison between EPI and FSE sequences in SNR
and CNR of tumor
The SNR was 7.99±2.51 in EPI sequence and 3.36±0.58
in FSE sequence, whereas the CNR was 5.51±2.02 in
EPI sequence and 2.21±0.79 in FSE sequence. Both re-
sults showed significantly higher values in EPI sequence
than in FSE sequence (Table 2).
Discussion
Virtually any combination of radio-frequency pulses
used in conventional pulse sequences can be used in EPI,
and spin-echo type or gradient-echo type are usually
adopted in clinical application. From these two types of
EPI sequence, we selected multishot spin-echo type, of
which the contrast resolution is high, because this type
of EPI is less sensitive to the motion artifact, susceptibility artifact caused by air-containing bowel loop in the
pelvis, and blood-flow artifact compared with gradient-
322
Table 1 Three-point scale assessed by three reviewers to
grade echo-planar imaging
(EPI) of normal anatomy.
FSE fast spin echo
Fig. 5a, b A 74-year-old man
with pathologically confirmed
non-malignancy in the prostate.
Paired axial sections by
a multishot echo-planar image
and b fast spin-echo image at
the level of prostate. Three reviewers judged visualization of
small vessels of periprostatic
venous plexus (arrows, a) to be
superior in a
Fig. 6a, b A 75-year-old man
with pathologically confirmed
prostate cancer (pathological
Gleason score 5). Paired axial
sections by a multishot echoplanar image and b fast spinecho image at the level of prostate. Three reviewers judged
prostate zonal anatomy to be
more definite in a than in b
Anatomic sites
Number
Venous plexus
Reviewer 1
Reviewer 2
Reviewer 3
Total
40
Prostate zonal anatomy
Reviewer 1
Reviewer 2
Reviewer 3
Total
32
Neurovascular bundle
Reviewer 1
Reviewer 2
Reviewer 3
Total
38
Seminal vesicle
Reviewer 1
Reviewer 2
Reviewer 3
Total
31
Comparison with FSE images
p
Better
Same
Worse
8
5
6
19
32
35
34
101
0
0
0
0
<0.0001
5
4
5
14
27
28
27
82
0
0
0
0
0.0001
1
1
1
3
31
32
33
96
6
5
4
15
0.0075
7
6
7
20
22
24
23
69
2
1
1
4
0.0015
323
Table 2 Signal-to-noise ratios
(SNR) and contrast-to-noise ratios (CNR) of prostate cancer
on echo-planar imaging (EPI)
and fast spin-echo (FSE) T2weighted images
a
p<0.0001 compared with FSE
Patient no.
1
2
3
4
5
6
7
8
9
10
11
12
Mean±SD
SNR
CNR
EPI
FSE
EPI
FSE
6.24
9.46
12.46
5.76
7.95
7.80
7.28
3.28
6.09
8.69
9.95
10.88
7.99±2.51a
3.80
3.35
3.60
2.80
4.10
2.56
2.83
3.16
3.16
3.47
2.99
4.53
3.36±0.58
4.38
10.26
6.61
7.01
4.89
4.16
5.34
6.81
2.66
4.04
3.82
6.16
5.51±2.02a
3.19
3.20
2.68
2.21
0.72
2.18
2.88
1.51
2.07
1.56
1.42
2.94
2.21±0.79
echo EPI [11, 15, 16]. It has been demonstrated that an
endorectal coil gives a better SNR and improved spatial
resolution for prostate imaging compared with the body
coil [17, 18]. On the other hand, an endorectal coil is often not well tolerated and increased susceptibility effects
associated with EPI have been reported to deteriorate the
quality of diffusion-weighted images of the prostate [19].
In the present study, an endorectal coil was not used because of its possible susceptibility effects on EPI MR
images.
The evaluation of the performance of T2-weighted
EPI and T2-weighted FSE imaging in delineating normal
prostate anatomy demonstrated that EPI was equivalent
to or better than FSE in the regions except for neurovascular bundle. The superiority of EPI in the imaging of
structures such as the periprostatic venous plexus and
seminal vesicle composed of small vascular complex or
fluid-filled tubules [20] may be attributed to its heavily
T2-weighted contrast and overall fat-suppression effect
[16, 21] induced by water selective-excitation for suppression of chemical-shift artifact. These characteristics
of EPI would also favor the visualization of prostate zonal anatomy since the peripheral zone of prostate is high
in water content with abundant glandular components
and less stroma [20, 22]. This is in contrast to uterine
zonal anatomy, which has been reported to be poorly visualized in multishot EPI compared with FSE imaging
[15]. In our study, glucagon was used to decrease the
motion artifact caused by intestinal peristalsis. This medication would also favor the improvement of the visualization. The reduction of delineation ability of EPI images in neurovascular bundle, which are visualized as low
signal intensity structures within fat tissues locating at 5
and 7 o’clock positions in the angle between the prostate
and the rectum, would have been caused by fat-suppression effect.
With regard to the detectability of prostate cancer in
the peripheral zone, both SNR and CNR of lesions were
significantly higher in EPI than in FSE. The high CNR
may reflect the property of EPI that the heavily T2weighted imaging enhance the subtle difference in water
content between the lesion and the surrounding peripheral zone tissue [20, 22]. Generally, the SNR of singleshot EPI images is lower than that of standard pulse sequences [16, 23], but a high SNR was obtained in the
present study, probably because of the reduction of susceptibility artifacts by increasing of the number of shots,
and using a large signal averagings; however, when the
same matrix size is used in FSE and EPI, the SNR may
be equivalent in both methods. Furthermore, these results are valid only for examinations performed with a
phased-array coil and that they cannot be extrapolated to
examinations performed with an endorectal coil. Approximately 70% of cases in prostate cancer arise in the
peripheral zone [24], and the accuracy of tumor detection for cancers originating in the peripheral zone using
MR imaging is reported to be approximately 50–70%
[7, 8, 9, 10]. The remaining prostate cancer cannot be
detected because the lesions were essentially isointense
to the peripheral zone [25]. The lesions of prostate cancer that were missed on MR images are reported to be
small in size [25, 26, 27, 28, 29] or poorly differentiated
[25, 26, 28]. Pariver [25] and Schiebler [26] reported
that poorly differentiated tumor have no defined boundaries and blend with normal prostate architecture, because of tending to infiltrate within the gland, resulting
in uniform signals for the prostate gland. On the other
hand, well to moderately differentiated carcinomas grow
in nodules of densely packed glandular elements with
little central space mucin storage; therefore, the high
cellularity and reduced fluid content of cancer generate
a low signal intensity. In the 2 patients with poorly differentiated adenocarcinoma examined in the present
study, both SNR and CNR of the tumors were high in
T2-wighted EPI, suggesting that some of the tumors of
which the signal intensity is the same as that of the surrounding prostate structures in T2-wighted FSE images
can be visualized by EPI.
324
The potential limitation of the present study is that
MR findings are not compared with the results of histological mapping of the prostate. We interpreted MR
lesions as prostate cancer from morphological criteria. It
has been reported that on MR images the low-SI cancerous areas appear as more round and triangular-formed lesions [10], whereas the hypointense benign tissue changes show more wedge-shaped, linear, stripy forms, and
diffuse extension without mass effect [10, 30]. It has also
been pointed out that the tumor detection in the peripheral zone on MR images differs according to size and location of the lesions [25, 26, 27, 28, 29]. In the present
study, we calculated SNR and CNR only in the lesions
that were larger than 5 mm in size, fulfilled the common
morphologic criteria of the prostate cancer, and located
in the posterior aspect of the outer gland. Furthermore,
locations of all these lesions were consistent with the estimation by TRUS-guided needle biopsy. Although even
the TRUS-guided needle biopsy is not a gold standard
for localizing cancer within prostate [31, 32], we believe
that our criteria for selecting the lesion could improve
the accuracy to a considerable degree.
In T2-weighted MR imaging, low signal intensity lesions in the peripheral zone do not represent a specific
finding for cancer because benign conditions, such as
prostatitis, hemorrhage, or dystrophic changes related to
radiation or androgen-deprivation therapy, can mimic
cancer [18]. This situation would more or less apply to
EPI T2-weighted imaging. The gradient-echo EPI may
be sensitive for detecting intraprostatic hemorrhage due
to susceptibility dephasing associated with hemorrhage.
On the other hand, the spin-echo EPI would be less sensitive because of its less sensitivity for susceptibility
changes. Indeed, the spin-echo EPI was not significantly
different from FSE in detecting susceptibility dephasing
associated with chronic intracranial hemorrhage, although the gradient-echo EPI showed higher sensitivity
[33].
In the present study for the comparison of T2-wighted
images between EPI and FSE, the patients in whom tumors were visualized in both images were examined. In
FSE, a 512 matrix can be used, but currently not in EPI;
therefore, the spatial resolution of EPI is lower than that
of FSE, and EPI would be inferior to FSE in evaluating
the precise extension of the tumor such as capsular invasion. However, because T2-weighted images using
multishot EPI has higher contrast resolution than that by
FSE in imaging of prostate cancer, it may be useful if
EPI sequence is additionally performed in patients in
whom the diagnosis of tumors by T2-weighted FSE images is difficult. Recently, some preliminary works have
demonstrated the utility of quantifying apparent diffusion coefficient to discriminate between normal and malignant prostate tissue [19, 34]. The combination with
this and another application of EPI imaging deserves further study. It has been reported that in 45.1% of the patients with impalpable PSA detected prostate cancer
(clinical stage T1c) was pathological stage pT3 [35]. The
EPI T2-weighted imaging would have the potential usefulness in the detection of such impalpable tumors.
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