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Urological Oncology
2010 BJU INTERNATIONAL
INCREASED PROSTATE CANCER DETECTION WITH MULTIPARAMETRIC MRI
DELONGCHAMPS
ET AL
.
BJUI
Multiparametric magnetic resonance
imaging for the detection and localization
of prostate cancer: combination of T2-weighted,
dynamic contrast-enhanced and diffusionweighted imaging
BJU INTERNATIONAL
Nicolas Barry Delongchamps*, Mathieu Rouanne*, Thierry Flam*,
Frédéric Beuvon†, Mathieu Liberatore‡, Marc Zerbib* and François Cornud‡
Departments of *Urology, †Pathology and ‡Radiology, Cochin Hospital, Paris Descartes University, Paris, France
Accepted for publication 25 May 2010
Study Type – Diagnostic (exploratory
cohort)
Level of Evidence 2b
What’s known on the subject? and What does the study add?
Dynamic contrast enhanced (DCE) and diffusion weighted (DW) MRI have demonstrated
their potential value in distinguishing malignant from benign prostate tissue, but none of
them used alone is capable of optimally characterizing tumours in the prostate.
The combination of DW, DCE and T2W imaging increased significantly MRI performance
for cancer detection in the peripheral zone.
OBJECTIVE
• To evaluate the combination of multiple
magnetic resonance imaging (MRI)
techniques, including T2-weighted imaging
(T2W), dynamic contrast-enhanced imaging
(DCE) and diffusion-weighted imaging
(DWI), for the detection and localization of
prostate cancer.
techniques combined were scored for the
likelihood of tumour in each area and results
were compared with whole-mount analysis.
• The area under the receiver operating
characteristic curve (Az) was used to evaluate
accuracy for tumour detection. The
association between MR accuracy and
Gleason score was statistically assessed.
• The Az value for T2W + DWI was
significantly higher than that for T2W + DCE
or for the three sequences combined.
• Gleason score was significantly associated
with cancer detection in the PZ.
CONCLUSIONS
PATIENTS AND METHODS
RESULTS
• In all, 57 patients underwent endorectal
MRI at 1.5 T before radical prostatectomy
(RP) for localized prostate cancer.
• On T2W images and histological wholemount analysis, the peripheral zone (PZ) and
transition zone (TZ) were divided into upper
and lower glands, as well as left and right
halves, thus yielding four quadrants for each
zone.
• On histological analysis, the total number
of tumour foci, their location and larger
diameter were recorded. T2W alone,
T2W + DWI, T2W + DCE and all three
INTRODUCTION
With the widespread use of PSA screening, up
to 80% of patients diagnosed with prostate
cancer are staged T1c. This downward stage
migration has led to the identification of
©
• Of the 456 prostate octants analysed, 145
showed cancer on whole-mount analysis,
120 (83%) of them with a diameter assumed
to correspond to a volume >0.2 cm3. Gleason
score was ≥7 in 68 (47%) tumours.
• In the PZ, the Az value was significantly
higher for T2W + DWI, T2W + DCE and all
three techniques combined than for T2W
alone (P < 0.05).
• In the TZ, the Az value was higher for
T2W + DWI than for T2W alone, but the
difference was not significant.
small and well-differentiated cancers at
radical prostatectomy (RP). These cancers,
designated as ‘clinically insignificant’ [1],
should probably not be managed with radical
and possibly morbid treatment. Development
of active surveillance and, more recently, focal
• Adding DWI and DCE to T2W imaging
increased MRI performance in cancer
detection in the PZ significantly.
• However, this multiparametric model
failed to improve performance in the TZ.
• Gleason score significantly influenced
cancer detection in the PZ but not in the TZ.
KEYWORDS
prostate cancer, detection, localization,
dynamic contrast-enhanced MRI, diffusionweighted imaging
ablation, has led clinicians to reconsider the
management of these patients. However, the
disease characteristics require to be better
clarified. Staging tools are therefore needed
to identify patients who can be managed
without radical treatment.
2010 THE AUTHORS
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2 0 1 0 B J U I N T E R N A T I O N A L | 1 0 7 , 1 4 11 – 1 4 1 8 | doi:10.1111/j.1464-410X.2010.09808.x
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D E L O N G C H A M P S ET AL.
The presence of adverse pathological features
on biopsy, high PSA level or PSA doubling
time, and/or suspicion of extracapsular or
seminal vesicle invasion on T2-weighted MRI
are clearly predictive of aggressive disease [2].
However, it is far more difficult to determine
precisely the number and location of tumour
foci within the gland. None of these staging
procedures offers an accurate prostate
mapping of the disease. Attempts at
histological mapping of the prostate have
been made with saturation transrectal and
transperineal prostate biopsies [3]. However,
correlation analyses with whole-mount
glands show that even these procedures can
miss up to 40% of cancer foci [3].
Prostate MRI has undergone several technical
improvements and is showing promise for
prostate tumour detection and localization. In
addition to morphological information, MRI
can analyse the physiological properties of
tissues. T2-weighted (T2W) MRI measurement
is dependent on free water abundance and
macromolecular environment. Diffusionweighted imaging (DWI) is sensitive to
restriction of water molecule diffusion [4],
and dynamic contrast-enhanced (DCE) MRI is
capable of assessing microvascular properties
[5]. All these techniques have shown their
potential value in distinguishing malignant
from benign prostate [4,5]. However, none of
them used alone is capable of optimally
characterizing tumours in the prostate.
Recent studies have showed that their
combination could reinforce and/or
complement each other [4,6]. On the other
hand, combining techniques of different
accuracy could also decrease their potential
detection value. The optimal combination of
large amounts of multiparametric imaging
data therefore remains a challenge. The
present study aimed to evaluate the
combination of multiple MRI techniques,
including T2W imaging, DCE and DWI for the
detection of prostate cancer.
PATIENTS AND METHODS
Between November 2008 and April 2009, 57
consecutive patients with biopsy-proven
prostate cancer underwent T2W MRI, DCE and
DWI before RP in our institution.
Magnetic resonance images were obtained
with a 1.5 T imager (Avanto, Siemens Medical
Systems, Erlangen, Germany) and an
integrated endorectal pelvic phased-array coil
1412
(MR Innerva; Medrad, Pittsburgh, PA, USA).
The endorectal coil was inserted and inflated
to a volume of ≈80–100 mL. The examination
started with a short biplane (20 s) localization
sequence to check the position of the rectal
coil and to ensure that the different
sequences would cover the whole prostate,
including the seminal vesicles. The threedimensional T2W fast spin-echo sequence
was then acquired (repetition time [TR]/echotime [TE], 1300/120; field of view [FOV],
18 cm, matrix, 186 × 256). It provided 224
images (voxel size, 0.8 × 0.8 × 1 mm) covering
the whole pelvis up to the aortic bifurcation.
DW images (TR/TE, 3700/104; FOV, 18 cm;
matrix, 186 × 256; slice thickness, 3.5 mm)
were obtained by using single-shot spin-echo
echo-planar imaging. Two b values (b0–b800)
were used and restriction of diffusion was
quantified by the apparent diffusion
coefficient (ADC) value. The orientation and
location of the images (20 slices) were
prescribed identically to the transverse T2W
prostate images. The gradient echo DCE data
sets (TR/TE/flip angle, 5.11/1.85/10; slice
thickness, 3.5 mm; temporal resolution, 8.5 s,
35 phases) were obtained after a bolus
injection of gadolinium (0.1 mmol/kg; rate of
injection, 3 mL/s, power injector, followed
by a 15 mL flush of saline) and transferred
to an independent workstation where a
pharmacokinetic model derived from the Tofts
model (iCAD, Nashua, Park Ridge, IL, USA) was
used to convert the variations of signal
intensity into variations of gadolinium
concentration. Pharmacokinetic variables
were determined, including Ktrans (forward
volume transfer constant), Kep (reverse reflux
rate constant between extracellular space and
plasma), and the area under the gadolinium
concentration curve (AUGC) in the first 60 s
after injection.
MRI PROSTATE MAPPING AND EVALUATION
OF DATA
Two experienced radiologists (FC, ML)
interpreted the MR images by consensus. They
were blinded to clinical (rectal examination),
biological (PSA value) and pathological results
(biopsy and RP specimen findings). The
peripheral zone (PZ) and the transition zone
(TZ) of the prostate were divided into upper
and lower glands, as well as left and right
halves, thus yielding four quadrants for each
zone and 576 areas for the whole series. The
limit between the upper and lower gland was
defined as the section running through the
widest transverse diameter of the prostate. As
detection and localization of prostate cancer
by functional MRI was the only goal of the
present study, assessment of extracapsular
extension was not taken into account. If the
focus was detected on more than one
sequence, the size of the tumour focus was
measured on the sequence showing the
largest diameter. On the T2W sequence, the
observers assigned a score to each focus
using a two-point scale: 0, benign; 1,
malignant. In the PZ, mass-like hyposignals
were considered as suspicious for cancer,
whereas heterogeneous patterns or nonmass-like hyposignals were considered as
benign. In the TZ, only homogenous,
anteriorly located and lenticular-shaped
hyposignals were considered as suspicious for
cancer [7]. According to the ADC value, the
observers assigned a three-point scale score:
0, benign (ADC > 1500); 1, indeterminate
(ADC = 1200–1500); 2, malignant
(ADC < 1200). For DCE MRI, the iCAD’s
pharmacokinetic analysis software used the
whole DCE curve that had 35 phases with
8.5 s temporal resolution and implemented
Tofts model. The default Weinmann arterial
input function (AIF) was used [8]. Based on
the brightness of the colour-coded value of
each parameter, the observers assigned a
three-point scale score: 0, benign (dark); 1,
intermediate (mid-bright); 2, malignant
(bright). The scores obtained were added
together to obtain a three-point scale for
T2W + DWI, a seven-point scale for
T2W + DCE, and a nine-point scale for all
sequences combined (Figs. 3-5).
HISTOLOGICAL EVALUATION
Radical prostatectomy specimens were fixed
overnight (with 10% neutral-buffered
formaldehyde) and coated with India ink.
Seminal vesicles were separated from the
prostate and processed separately. The glands
were cut into 4-mm sections perpendicular to
the posterior plane, labelled, embedded in
paraffin, and further sectioned to produce 5μm whole-mount sections that were stained
with haematoxylin and eosin. A single
pathologist (FB) microscopically reviewed all
samples. The total number of tumour foci and
their location were recorded. An area of
carcinoma was considered a separate focus if
it was separated by a low-power field
diameter (4.5 mm) from the nearest adjacent
focus. Each tumour focus was graded
according to the modified Gleason grading
system [9]. The volume of each tumour focus
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INCREASED PROSTATE CANCER DETECTION WITH MULTIPARAMETRIC MRI
N (%)
Rectal examination
Normal
Suspicious
Number of prostate cancer cases
Number of prostate areas analysed
Number of tumour foci
In the PZ
In the TZ
Gleason score
Gleason ≤ 6
Gleason ≥ 7
Tumor diameter (>7 mm)
In the PZ
In the TZ
43 (76)
14 (24)
57
456
FIG. 1.
Comparison of ROC curves
between T2W (T2) imaging alone,
T2W + DCE (T2_DCE), T2W + DWI
(T2_DWI) and all three techniques
combined (T2_DWI_DCE) for
cancer detection in the PZ.
100
80
Sensitivity
TABLE 1 Clinical and pathological
characteristics of the 57 prostate cancers
60
40
112
33
20
T2
T2_DWI
T2_DCE
T2_DWI_DCE
77 (53)
68 (47)
0
91 (81)
29 (91)
0
TABLE 2 Sensitivity and specificity of MRI for the detection of prostate cancer, when using the optimal
score thresholds
Sensitivity, % (95% CI)
Specificity, % (95% CI)
T2W alone
T2W + DCE (>4/7)
T2W + DWI (>1/3)
T2W + DCE + DWI (>5/9)
63 (53–73)
79* (69–87)
81* (72–88)
80* (70–87)
98 (97–100)
92 (86–96)
93 (87–97)
97 (93–99)
T2W alone
T2W + DCE (>6/7)
T2W + DWI (>2/3)
T2W + DCE + DWI (>6/9)
71 (52–85)
47* (30–65)
71 (52–85)
53* (30–65)
98 (95–100)
77* (71–83)
98 (95–100)
83* (77–88)
PZ
TZ
*P < 0.05 vs T2W alone (McNemar test).
was estimated according to its larger
diameter. A diameter >7 mm was considered
to correspond to a tumour volume >0.2 cm3
[10].
MEASUREMENTS AND STATISTICAL ANALYSIS
Each pathological whole-mount section was
matched to a corresponding MR image on the
basis of the location of the ejaculatory ducts,
the diameter of the prostate and the
approximate distance from the base or apex. A
correlation analysis between the MRI and
pathological findings was then performed in
each of the eight previously defined prostatic
regions. Only tumours with diameter >7 mm
©
Az: 0.81; 95%CI: 0.75–0.86
Az: 0.92; 95%CI: 0.88–0.96
Az: 0.91; 95%CI: 0.86–0.94
Az: 0.92; 95%CI: 0.88–0.95
were considered for the correlation analysis.
Receiver operating characteristic (ROC) curves
and the corresponding areas under the ROCs
(Az) were estimated non-parametrically for
the detection of cancer with T2W alone,
T2W + DWI, T2W + DCE, and a combination of
the MRI sequences. These Az values were
compared using a pairwise comparison of
ROC curves. Sensitivity and specificity of each
MRI combination were calculated and
compared using the McNemar test. The chisquared test, which accounts for qualitative
variables, was used to compare Gleason score
(Gleason <7 vs ≥7) between tumours detected
and missed by MRI. All statistical tests
were two-sided, and P values <0.05 were
considered to indicate statistical significance.
20
40
60
100-Specificity
80
100
Statistical analyses were performed using
MedCalc® software, version 11.0.0.0.
RESULTS
The 57 patients included in the analysis had
a median (range) age of 63 (54–76) years
and a median (range) PSA level of 7 (2.8–28)
ng/mL. Their clinical and pathological
characteristics are summarized in Table 1.
Of the 145 cancer foci identified on wholemount analysis, 120 (83%) had a diameter
>7 mm, corresponding to an estimated
volume >0.2 cm3. Gleason score was ≥7 in
53% (53/112) of PZ tumours vs 27% (nine
of33) of TZ tumours (P = 0.01).
MRI PERFORMANCE FOR CANCER DETECTION
IN THE PZ
The Az values (Fig. 1) for T2W + DWI,
T2W + DCE and all three sequences combined
were significantly higher than that for T2W
alone (Table 1, P = 0.003, 0.03 and 0.009,
respectively). Although T2W + DWI performed
better than T2W + DCE, the difference was
not significant (P = 0.8). When using the
optimal thresholds for determining the
presence of cancer, the three MR sequences
combined had the highest sensitivity (80%)
and specificity (97%) for cancer detection in
the PZ (Table 2). A Gleason score ≥7 was
associated with greater MRI performance
with all the sequence combinations
(P < 0.001).
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D E L O N G C H A M P S ET AL.
MRI PERFORMANCE FOR CANCER DETECTION
IN THE TZ
80
Sensitivity
The Az for T2W + DWI was higher than that
for T2W alone, but the difference was not
significant (Fig. 2, P = 0.4). Interestingly,
T2W alone performed significantly better
than T2W + DCE (P = 0.002) as well as all
three sequences combined (P = 0.03).
As a result, the combination of either
T2W + DCE or all three MR sequences
significantly decreased sensitivity and
specificity (Table 2). Gleason score did not
influence MR performance for any of the
sequence combinations (P > 0.1).
FIG. 2.
Comparison of ROC curves
between T2W (T2) imaging alone,
T2 + DCE (T2_DCE), T2 + DWI
(T2_DWI) and all three techniques
combined (T2_DWI_DCE) for
cancer detection in the TZ.
100
60
40
20
T2
T2_DW
T2_DCE
T2_DW_DCE
Az: 0.84; 95%CI: 0.79–0.89
Az: 0.88; 95%CI: 0.83–0.92
Az: 0.70; 95%CI: 0.63–0.76
Az: 0.75; 95%CI: 0.69–0.80
0
0
DISCUSSION
Even if T2-weighted MRI shows a high
sensitivity for large-volume tumours [11,12],
its accuracy for detection of smaller foci is
less well established [13]. In patients with
palpable cancer, sensitivity has been reported
to be as high as 96% [11]. The real issue,
however, is how to detect small confined
tumours albeit of substantial volume (>0.2–
0.5 mL). Patients with palpable cancer, high
PSA level and adverse biopsy results do not
present any challenging staging problem to
clinicians. In comparison, patients free of any
adverse prognostic factor are potential
candidates for focal ablation or active
surveillance and need further staging to
ensure the absence of large-volume or
multifocal disease. For these patients, T2W
imaging sensitivity for cancer detection in
the PZ may not exceed 20% [13,14]. In this
setting, T2W imaging might only be helpful in
detecting extracapsular extension, seminal
vesicle invasion or large intracapsular
tumours close to the capsule. As a result,
small, albeit significant, tumours, possibly
multifocal and high-grade, could remain
under-staged. In the TZ, T2W imaging
accuracy for cancer detection was reported to
be even worse. Although TZ tumours tend to
be less aggressive [15], they can account for
up to 30% of cancers. One large series of
anterior gland cancers showed that MRI
missed 78 of 79 tumours with a volume
>0.5 mL [16]. However, more recent reports
showed a higher accuracy in the TZ. Using
validated criteria for T2W imaging cancer
detection in the TZ (anterior homogeneous
hyposignal, ill-marginated, lenticular shape)
[7], different authors [10,17–19] subsequently
reported sensitivities and specificities
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20
40
60
100-Specificity
ranging between 24–68% and 91–99.9%,
respectively.
To improve the limited accuracy of T2W
imaging, other MR techniques have been
developed, including DCE and DWI. In the PZ,
DCE MR imaging demonstrated high accuracy
for the detection of tumour foci >0.5 cm3
[18,20–22]. However, most of the smaller
foci remain undetected [17,23]. In the TZ,
limitations of DCE MRI are even higher
because of the similar kinetics of gadolinium
enhancement in BPH and prostate cancer
[24]. More recently, several studies have also
suggested the potential benefit of DWI in
detecting prostate tumours. The ADC values,
which measure the restriction of water
molecule diffusion within tissues, were
reported to be significantly lowered in
malignant vs benign tissue in the PZ [4]. In the
TZ, however, ADC values of BPH are in the
range of those of prostate cancer [4,24],
making DWI of poor diagnostic value in this
prostatic area.
Owing to the limitations of functional
sequences used separately, several authors
[6,24–27] suggested that a multiparametric
assessment of prostatic tissue, including T2W,
DW and DCE imaging, could improve the
overall MRI sensitivity and/or specificity. This
combination, however, is challenging. The
main difficulty lies in how to take into
account the different data provided by each
of the MR techniques. In particular, if the
results of the different techniques disagree
80
100
with each other, which should be given more
credit? Should data provided by each
technique be balanced according to the
assumed accuracy of each technique taken
separately? In our study, all variables
combined were balanced equally for the
interpretation of results: T2W, ADC, Ktrans, Kep
and AUGC values had the same impact
with regard to data interpretation. This
methodology might not provide the optimal
results, however, and highlights the
difficulties presented by a multiparametric
model. This issue was recently assessed
by Langer et al. [6]. Using a stepwise
regression model, they tested and compared
four MRI quantitatively measured variables,
including T2W-relaxation time, ADC value,
Ktrans and Kep to evaluate which of them
provided the best performance for cancer
detection in the PZ. The optimal
multiparametric model consisted of
combining ADC, T2W and Ktrans. However,
they also found that ADC was the bestperforming single variable. Although the
three variables combined tended to be better
than ADC alone, the difference was not
statistically significant (P = 0.09). These
findings could suggest that the ADC value
should be given more power if included in a
multiparametric model.
The results of the present study suggest that
DW and DCE imaging, when combined with
an equally balanced power to T2 imaging,
add significant accuracy in the PZ compared
with T2 alone. Using all three techniques
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INCREASED PROSTATE CANCER DETECTION WITH MULTIPARAMETRIC MRI
FIG. 3. Hypovascular TZ cancer. T2W MRI (top panels): anterior lenticular hyposignal, ill-marginated,
anteriorly located in the transition zone. DWI (middle panels): low ADC value in the same area (arrows). DCE
MRI (bottom panels): low value of the dynamic variables on a qualitative visual assessment. Histological
examination: Gleason score 6 carcinoma (Ca) (arrows).
making their detection more difficult with
DCE imaging. In the present study, most of
the TZ tumours had a low Gleason score,
which may explain the poor sensitivity
of DCE.
In the present study, we excluded small
tumour foci (diameter <7 mm) from analysis
because they are probably not a clinical issue.
Usually considered as ‘clinically insignificant’,
they are missed by all MRI sequences, used
either alone or in combination. ‘Inapparent
tumours’ on MRI are characterized
histologically by sparse and low-grade
tumour cells intermixed with healthy tissue
[30]. The ratio of tumour cells to healthy
tissue in these foci may not reach 60% [30].
These histological considerations might be of
great interest if tumour cell density appeared
to be correlated with cancer progression,
which to our knowledge has not yet been
reported. If so, MRI could become a strong
predictor of either the absence of cancer or
the presence of non-aggressive inapparent
tumours.
combined, we reached a sensitivity of 80%
and a specificity of 97% for the detection
of tumour foci >0.2 mL. DW imaging
seemed to add more performance to our
multiparametric model than DCE, as has been
suggested before [6].
In the TZ, combined MR sequences failed to
improve cancer detection. Interestingly, DCE
imaging decreased accuracy significantly, and,
as a result, the performance of all three
techniques combined. Although DWI added
©
accuracy to T2W alone, the difference was not
significant. These results are consistent with
those of Haider et al. [4] and suggest that
morphological criteria described on T2W
imaging are still the gold standard for the
detection of TZ cancer. Although the low
accuracy of DCE in the TZ is an established
finding [17,18,28], it may not alone explain
why the combination of DCE + T2W reached
so low a sensitivity (47%). As suggested by
one study [29], low-grade tumours have less
vascular density than high-grade tumours,
The present study had several limitations, one
of them being the population studied. For the
correlation analysis, we did not select
exclusively low-risk patients according to PSA
level, rectal examination and biopsy results.
These low-risk patients are considered as the
potential candidates for focal tumour
ablation or active surveillance, for which MRI
combination techniques would be of staging
value. Additionally, we did not include MR
spectroscopic imaging in our multiparametric
model, although it does not improve, at 1.5 T,
the accuracy of T2W imaging for cancer
detection in the PZ (Az, 0.60 vs 0.58,
respectively; P > 0.05) [31]. Nevertheless,
spectroscopy with high-field 3 T magnets is
currently being investigated and might show
promise in detection of prostate cancer.
Finally, whole-mount analysis of RP
specimens focused on tumour foci alone,
therefore excluding other lesions, such as
prostatitis infiltrates, that can simulate cancer
on MRI. Consequently, we were unable to
analyse the nature of false-positive images
identified on MRI examination.
In conclusion, adding DWI and DCE to
T2W imaging significantly increased MR
performance for cancer detection in the PZ.
However, this multiparametric model failed to
improve performance in the TZ. Gleason score
significantly influenced cancer detection in
the PZ but not in the TZ.
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D E L O N G C H A M P S ET AL.
FIG. 4. Prostate cancer originating in the PZ. Bilateral hyposignal on the T2W image (arrows, T2) with a low value of the ADC (arrows, ADC), high K trans (vascular
permeability, Ktrans) and Kep (washout, Kep) values, but low AUGC value (arrows, AUGC).
FIG. 5 Anterior cancer originating in the TZ. Homogenous and anteriorly located TZ hyposignal on the T2W sequence (arrow, T2), with low ADC value and high values
of dynamic variables (Ktrans, AUGC and Kep).
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CONFLICT OF INTEREST
None declared.
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Correspondence: Nicolas Barry
Delongchamps, Department of Urology,
Hôpital Cochin, 27 rue du Faubourg Saint
Jacques, 75014 Paris.
e-mail: [email protected]
Abbreviations: ADC, apparent diffusion
coefficient; AUGC, area under the gadolinium
concentration curve; DCE, dynamic contrastenhanced imaging; DWI, diffusion-weighted
imaging; PZ, peripheral zone; ROC, receiver
operating characteristic; RP, radical
prostatectomy; T2W, T2-weighted imaging;
TZ, transition zone.
©
BJU INTERNATIONAL
©
2010 THE AUTHORS
2010 BJU INTERNATIONAL