J. Exp. Clin. Cancer Res., 24, 4, 2005
MR Spectroscopy of Prostate Cancer. Initial Clinical Experience
E. Squillaci, G. Manenti, S. Mancino, M. Carlani, M. Di Roma, V. Colangelo, G. Simonetti
Dept. of Diagnostic Imaging and Interventional Radiology, University "Tor Vergata", Rome, Italy
Aim of the study was to evaluate the effectiveness of proton MR Spectroscopic (MRS) imaging in the detection
and localization of prostate cancer, prospectively compared with histopathologic findings. Magnetic Resonance
(MR) and MRS imaging were performed in 65 patients with high levels of prostate-specific antigen (PSA) and
suspicious areas at the transrectal ultrasound (TRUS). At MR areas of interest were reported as normal, equivocal or suspicious. At MRS imaging, cancer was diagnosed as "possible" if the ratio of choline plus creatine to citrate exceeded 2 SDs above mean normal peripheral zone values or as "definite" if the ratio exceeded 3 SDs. All
patients underwent a TRUS 10-core biopsy within 30 days of the imaging study. MR alone showed sensitivity,
specificity, positive predictive values, negative predictive values and accuracy for detection of prostate cancer of
85%, 76%, 53%, 91% and 65%, respectively, whereas MRS alone showed 89%, 77%, 78%, 69% and 83%, respectively. These values were 71%, 90%, 89%, 74% and 80% when the prostate was evaluated combining MR
and MRS. The addition of MRS to the MR imaging provides a higher specificity in tumour detection and can be
recommended as a problem-solving modality for patients with elevated PSA levels and suspicious TRUS before
biopsy.
Key Words: Prostate, Prostatic cancer, Biopsy, Magnetic Resonance Imaging, Magnetic Resonance
Spectroscopic Imaging
Prostate carcinoma is an important medical and
socio-economical problem due to its increasing incidence among the male population and the steady ageing of the western countries. The American Cancer
Society estimated 230,000 new cases of prostate carcinoma and 29,900 cases of related deaths in the
United States in 2004 (1).
A yearly test of the PSA levels combined with a
digital rectal examination (DRE) and a transrectal
ultrasonography (TRUS) completed with a biopsy (2)
have allowed the detection of cancer at an earlier
stage compared to the past. This has enabled the use
of treatments such as brachytherapy, intensity-modulated radiotherapy, thermal ablation or cryosurgery
that are less aggressive and show less morbidity than
radical prostatectomy. It is, therefore, of the outmost
importance the precise localization and staging of the
neoplasm to evaluate its biological aggressiveness.
Magnetic Resonance (MR) imaging allows a better definition of the morphology and of the anatomy
of the prostate gland. To date, however, the diagnos-
tic accuracy varies widely between authors ranging
from 75 to 90% and reaching a 97% (3) in the detection of known lesions, but showing a lower accuracy
in case of lesions smaller than 5 mm (4). The morphologic imaging alone, however, has a low specificity (55%) (5). In fact, prostatitis, post-biopsy
bleedings or the effects of therapy may show a characteristic low intensity signal in the T2 weighted
sequences thus mimicking the neoplastic lesion.
The introduction of the 3D Magnetic Resonance
Spectroscopic (MRS) imaging has enabled the correlation of both anatomical and morphological data with
functional informations about tissue metabolism.
Combined MR/MRS imaging studies show more accuracy in the detection of prostate cancer enabling the
simultaneous displaying of both extension and biological aggressiveness (6). Purpose of this study was to
define the effectiveness of MRS imaging compared to
MR imaging in the detection and localization of prostatic neoplastic foci prospectively assessed with postbiopsy histopathological examination.
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Materials and Methods
Patients. Between April 2004 and January 2005,
65 consecutive patients (mean age 68.5 years, range
55-82) underwent MR and MRS of the prostate.
Inclusion criteria were: a) free-PSA level higher
than 4.0 ng/ml or; b) suspicious (<15%) free-to-total
PSA ratio measured by immunoassay 20 days prior to
MR. Patients included in the study had a mean free
PSA value of 24.15 ng/ml (range 4.3-44 ng/ml).
Patients (with unknown prostate cancer) were
referred for MR with evidence of focal or diffuse
hypoechoic lesion/s at TRUS performed up to 10 days
before MR.
Informed consent was obtained from all patients
before MR imaging.
MR Technique. MR imaging was performed with a
1.5 T scanner (Philips Gyroscan Intera, Best, The
Netherlands) with 30 mT/m gradients by using the
body coil for radiofrequency (RF) excitation and a
surface coil (C1) placed on the pubic region for signal acquisition. To reduce bowel peristalsis and
improve imaging quality 1 mg glucagon (Glucagen;
Novo Nordisk, Mainz, Germany) or 20 mg
butylscopolamine (Buscopan; Boehringer, Ingelheim
am Rhein, Germany) were administered before imaging.
Morphologic study was obtained with high-spatial-resolution sagittal T2-weighted turbo spin-echo
(TSE) sequences to assess coil position, then coronal
and axial T2-weighted TSE images were obtained
from the apex to the seminal vesicles with the following parameters: repetition time/echo time msec
(TR/TE) 4.000/130 msec, 2.5 section thickness, no
intersection gap, 6 signal acquired (NSA), 19-cm
field of view (FOV), 240 and 256 (acquisition and
reconstruction) matrix, scan time 8:47 min. T2weighted with fat suppression (SPIR) sequences were
also obtained (4.750/90 msec TR/TE). The morphologic study was completed with 1H-MRS imaging and
dynamic contrast-enhanced MR (DCE-MR) imaging.
3D MR spectroscopic imaging volume was selected on the high-spatial-resolution axial T2-weighted
images. The sequence applied was the point resolved
spectroscopic (PRESS) with the following parameters: TR 1.600 msec, TE 136 msec (echo delay optimized) for quantitative citrate and choline multivoxel
detection, spectral bandwidth 1.000 Hz, 512 points,
FOV 14-cm, n. image 4, scan resolution 16, voxel
spatial resolution 0.24 cm3, scan time 17:25 min.
Band-selective inversion with gradient dephasing
524
(BASING) sequence was used for the optimal water
and lipid suppression.
DCE-MR imaging was performed after the spectroscopic acquisition in all patients with fast field-echo
(FFE) T1-weighted sequence and 20 mL /sec singledose bolus injection of gadopentate dimeglumine (GdDTPA, Magnevist®; Schering, Berlin, Germany) with
the following parameters: TR 20 msec, TE 5 msec, flip
angle 20°, slice thickness 3 mm, FOV 18-cm, scan
number 10, scan time 2:57 min. These sequences were
used to show the contrast media uptake for the evaluation of quick contrast-enhancement of the peripheral
zone, synchronous with the central gland suggesting
neoangiogenesis of the lesion.
MR imaging and MRS imaging data analysis.
Images were examined by an expert radiologist (E.S.)
aware of the TRUS findings. Only morphologic
images included in the MRS imaging were evaluated
to allow a direct comparison between MR and MRS
imaging. Peripheral zone limits were assessed on the
axial T2-weighted where the prostatic capsule and
pseudo-capsule characteristically show a low-intensity signal band (7).
The presence of a peripheral zone neoplasia was
evaluated basing on the following criteria: 1) the
absence of low-intensity signal areas was considered
a normal pattern; 2) the presence of a non-homogeneous low-intensity signal area with irregular edges
or more triangular streaky lesions was considered
equivocal; 3) the presence of a homogeneous lowintensity signal smudgy-appearing area with rounded
sides and blurred outlines was considered highly suspicious for neoplasia.
Single voxels of the spectroscopic selected volume sequence were two-dimensionally plotted on a
grid superimposed on the related T2-weighted axial
images. The spectra related to the prostatic metabolites were automatically generated with the manual
pointing of ROIs (Region of interests) for each voxel
represented on the grid. Voxels with abnormal contrast-enhancement in the dynamic sequences were
further analyzed (Fig.1).
The integral values of the areas under the peak of
the prostatic metabolites citrate, choline and creatine
were calculated using a dedicated software for the
spectroscopic analysis, after frequency and baseline
correction. To detect the presence of prostatic cancer
the ratio of the integral values of choline plus creatine
to citrate (Cho+Cr/Cit) was calculated for each voxel.
"Possible" presence of carcinoma was defined when
this ratio was greater than 2 standard deviations (SDs)
MR Spectroscopy of Prostate Cancer
Fig. 1 - Dynamic contrast-enhanced axial T1-weighted FFE images: acquisitions before (A) and 20 seconds after contrast media injection (B) show an area of early wash-in Gd-DTPA contrast enhancement in the middle-left peripheral zone (arrow). In the acquisition after 45 seconds (C) the high intensity signal increases (arrow) compared with the remaining peripheral zone. After 120
seconds there is a synchronized Gd-DTPA wash-out of the peripheral zone lesion and of the adenomyoma (D).
compared with normal prostatic tissue (>0.75);
whereas a ratio greater than 3 SDs compared with
normal tissue (>0.86) was defined as "definite" cancer. Voxels with ratio values lower than 0.75 were
defined as normal tissue (8).
Suspicious or equivocal areas at the morphological imaging and voxels with (Cho+Cr/Cit) ratio >3
SDs and between 2 and 3 SDs were spatially assigned
to different regions of the prostate gland: apical,
intermediate, lateral and basal region for each side.
This kind of subdivision was used to correlate MR
and MRS imaging results with the histopathologic
findings (Fig.2).
Prostatic Biopsy. Each patient underwent systematic US-guided prostatic biopsy (trans-perineal) performed with an ATL (Advanced Technology Laboratories) HDI 5000 SonoCT Diagnostic Ultrasound
Machine with convex 7.5 MHz sector probe within 30
days from the spectroscopic session.
In all patients, a 10-core biopsy was performed
according to the octant subdivision of the prostate
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cious, >3 SDs and >2 - <3 SDs) and negative (normal
and < 2 SDs).
DCE-MR imaging data were not used for the statistical analysis.
Results
Fig. 2 - Coronal view scheme of the subdivision of the prostate
gland. This scheme was used to correlate the MR and
MRS imaging findings with the biopsy results.
gland (1 sample from the apex, the intermediate zone
and the basal region, 2 samples from the lateral zone,
for each side).
At least 2 samples were obtained from the suspicious zone or from the area showing pathologic characteristics at MR and MRS.
This additional sampling was used to compensate
for the inaccuracy in the correlation between the sextant biopsy technique and the morphologic and "voxelby-voxel" spectroscopic imaging. All samplings were
performed using a BioPince® Full Core Biopsy Gun
with an 18 gauge needle (MD Tech., Florida, USA).
Specimens were classified referring to the biopsy
sites and then an individual histological analysis for
each sample site was performed.
Each biopsic specimen was analyzed by a single
pathologist specialized in prostatic pathology.
Statistical Analysis. All data were analyzed using
the Statistical Package for Social Sciences, (SPSS®
V.12, Chicago, Illinois). On the basis of the
histopathological results, MR imaging, MRS imaging
and the combination of MR and MRS imaging
(MR/MRS) findings were encoded in descriptive statistics including sensitivity, specificity, accuracy and
positive (PPV) and negative (NPV) predictive value.
The Pearson χ2 test was used for the evaluation of the
statistical significance (p < 0.05) of the single techniques and their combination, compared with the
histopathologic finding.
For the statistical analysis the imaging results,
classified as normal, equivocal or suspicious, were
divided in two groups: positive (equivocal and suspi526
In 43 out of the 65 patients (66%) a focal or diffuse
low-intensity signal area was detected, mono- or bilaterally in the axial T2-weighted images, whereas in the
remaining 22 patients (34%) no pathologic distortion
of the intensity signal was detected. Particularly, the
morphologic findings of the MR imaging were correlated to the spatial localization of the prostate gland,
with 8 suspicious areas in the apex (5 left side, 3 right
side), 13 in the intermediate zone (4 left side, 9 right
side), 15 in the lateral zone (8 left side, 7 right side)
and 7 in the basal region (3 left side, 4 right side).
Of the 43 patients with suspicious neoplastic
lesions, 28 (65% true-positive TP) had histopathologic confirmation of adenocarcinoma, whereas 15 (35%
false-positive FP) had diagnosis of benign lesions (9
prostatitis and 6 nodular benign hyperplasia).
Of the 22 patients without suspicious images at
MR imaging, 17 (77% true-negative TN) had
histopathologic confirmation of the absence of malignant lesions (10 cases of chronic prostatitis, 7 cases of
nodular benign hyperplasia), whereas the remaining 5
patients (23% false-negative FN) had diagnosis of
adenocarcinoma.
On the basis of these results, MR imaging has
shown a sensitivity equal to 85%, a specificity of
53%, PPV 65%, NPV 77% and an accuracy of 69%
with a p value 0.013 (Table II).
MRS imaging has detected pathologic spectra
(Cho+Cr/Cit ratio > 3 SDs or >2 - <3 SDs) in 28 (43%)
patients, whereas in 37 (57%) the spectral analysis has
produced no-pathologic ratios (Cho+Cr/Cit < 2 SDs).
Suspicious areas were also related to the spatial
octant partitioning of the prostate gland therefore
allowing the detection of 3 areas with pathologic
ratios in the prostatic apex, 12 in the intermediate
zone (7 left side, 5 right side), 11 in the lateral zone
(5 left side, 6 right side), 2 in the basal region.
Of the 28 patients with Cho+Cr/Cit pathologic
ratio, 25 (89% TP) confirmed the presence of adenocarcinoma (Fig.3), whereas 3 (11% FP) were diagnosed as benign lesions (2 cases of chronic prostatitis, 1 case of nodular benign hyperplasia).
In the 37 patients with Cho+Cr/Cit < 2SDs, 29
(78% TN) generated histopathologic findings of
MR Spectroscopy of Prostate Cancer
benign lesion (18 cases of prostatitis and 11 cases of
nodular benign hyperplasia) (Fig.4) while in the other
8 patients (22% FN) a diagnosis of adenocarcinoma
(Table I).
MRS imaging demonstrated a 76% sensitivity,
91% specificity, 89% PPV, 78% NPV and an 83%
accuracy with a p value of 0.000 (Table II).
MR imaging combined with MRS imaging results
showed a sensitivity equal to 71%, a specificity of
90%, PPV 89%, NPV 74% and an accuracy of 80%
with a p value of 0.000 (Table II).
No significant correlations were found between
the MR and the MRS results and the bioptic sampling
findings, except in case of MRS imaging results and
histopathologic findings for the intermediate and lateral zones (p = 0.003 and p = 0.002, respectively).
Discussion
Nowadays, prostatic cancer represents the most
common cause of cancer-related death in the male
population (1).
Despite the high mortality rate, many cases of
prostate cancer are subclinical and accidentally
detected at autopsy (9).
Fig. 3 - Sagittal (A) and axial (B, C) T2-weighted images of the prostate showing a peripheral middle-right area of low intensity signal.
The spectrum obtained from this area shows elevated levels of choline and reduced levels of citrate, a pattern consistent with definite cancer (D). Histopathologic analysis confirmed the neoplastic nature of the lesion.
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E. Squillaci et al.
Fig. 4 - Axial T2-weighted images of the prostate showing an area of low intensity signal in the left peripheral zone (A, B, C). The MRS
spectrum demonstrated choline and citrate levels indicative of normal tissue (D). Post-biopsy histopathologic analysis showed
the absence of neoplastic cells in this area, confirming what MRS had correctly demonstrated whereas MR imaging findings
could have been misleading.
The available non-invasive diagnostic techniques
have large limitations in discriminating between
latent and aggressive or progressive neoplastic
lesions (10,11).
Olson et al. demonstrated that TRUS depicts up to
30% of palpable DRE lesions (12). In addition, these
authors showed that this technique has a high level of
FP because only 20% of hypoechoic lesions are
malignant. US-guided biopsy has also a high percentage of sampling errors due to the small part of the
prostatic gland effectively analyzed.
Thus, so many patients with abnormal PSA levels
(>4ng/ml) that undergo systematic sextant biopsies
528
have negative results and, therefore, need to be subjected to repeated biopsy (13,14).
The development of new therapies for prostatic
cancer, less invasive than radical prostatectomy,
requires detailed localization and the assessment of
the extent of the disease to be able to treat the patients
with a targeted therapy. This kind of approach
increases the therapy effectiveness and reduces the
related morbidity.
The detailed knowledge of the lesion location significantly helps patients with persistent elevated PSA
levels that undergo repeated biopsies.
MR has demonstrated a good sensitivity (78%)
MR Spectroscopy of Prostate Cancer
Table I - Correlation of MR imaging, MRS and biopsy findings
Biopsy findings
Negative
Positive
Total
MR
MRS
Negative Positive
Negative Positive
17
5
22
15
28
43
29
8
37
3
25
28
and a low specificity (55%) in the detection of neoplasm site/neoplastic foci due to the high percentage
of FP (post-biopsy bleedings, inflammation, fibrosis
etc.) (15).
The combination of metabolic data using the spectroscopic imaging add information to the morphologic imaging in the detection, staging, size evaluation
and assessment of the degree of aggressiveness of the
neoplasia (8,16,17).
However, most experiences are the result of retrospective studies where diagnostic accuracy of the MR
and MRS imaging was assessed on the basis of the
histopathologic data after radical prostatectomy.
The purpose of this study was to evaluate the MR
and MRS imaging capability in the detection and
detailed localization of prostate cancer. Every single
technique result was prospectively compared with
bioptic findings. Surface coil was used to avoid the
scarse tolerability and the typical artifacts of the
endorectal coil (18).
MR imaging has demonstrated an 85% sensibility
and a 53% specificity in detecting prostate cancer in
accordance with previous studies (8). MRS imaging
has shown high specificity in depicting prostate cancer compared to the MR (91% against 53%).
MR and MRS imaging results suggesting the presence of prostate cancer, resulted in high probability to
be neoplastic lesions (PPV 88%); otherwise, a negative
result excludes the presence of prostate cancer with
lower probability (77% NPV) due to the number of
FN. These may be ascribed to the typical feature for the
1.5 T magnetic fields high nominal value (0.24cm3) of
the voxel, with overlapping of the pathologic and notpathologic data in the same sampled voxel.
Furthermore, the limited aggressiveness of some
carcinomas may explain the lack of detection of the
neoplastic lesions at the MRS imaging. This has been
already described by some authors who have demonstrated that small tumors with low grade differentiation
Table II - Sensitivity, specificity, PPV, NPV, accuracy of
MR, MRS and combined MR/MRS imaging
Sensitivity
Specificity
PPV
NPV
Accuracy
MR (%)
MRS (%)
MR/MRS (%)
85
53
65
77
69
76
91
89
78
83
71
90
80
89
74
(Gleason 4 and 5) may be missed because of the slight
modifications of the citrate and choline levels (19).
Initial results with the 3T MRS imaging in
prostate cancer patients offer higher signal-noise ratio
(SNR) (20,21) and more accurate spectral resolution
with increased accuracy in the spatial detection of the
metabolic data (22,23).
Inadequate correlation between the MR/MRS
imaging and the histopathologic findings as to the
spatial localization of the lesions impairs the ability
of our study to demonstrate if tumor localization
affects the two imaging techniques to detect it (24).
That is directly related to the fact that the US-guided
biopsies do not assure an exact correspondence
between bioptic sites and the suspicious areas at the
MR and MRS imaging. Only radical prostatectomy
results can afford to definitely answer this question.
In conclusion, this initial study, performed on a
small population, demonstrates that MR/MRS imaging might be indicated in patients with elevated PSA
levels and TRUS findings suspicious for neoplasia,
who are candidate to bioptic sampling. In view of the
excellent feasibility of these two techniques performed with a surface coil, this imaging session provides new important information to those patients
with random bioptic findings negative for pathologies
and persisting elevated PSA levels that are candidate
to a second bioptic sampling.
The detection of suspicious areas at the MR and
MRS imaging offers the potentiality to perform targeted MR-guided biopsies (25,26) without the need
to compare MR imaging and TRUS findings (24).
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Received: June 16, 2005
Prof. Ettore Squillaci
University of Rome "Tor Vergata"
P.T.V. Viale Oxford, 81
00133 Rome, Italy
Tel.: +39 06-20902401; Fax: +39 06-20902404
E-mail: [email protected]