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Genitourinary Imaging |
1 Department of Radiology, University of California, San Francisco, 505
Parnassus Ave., San Francisco, CA 94143-0628.
2 Present address: Department of Radiology, University of Utah, 30 N 1900 East,
#1A71, Salt Lake City, UT 84132-2140.
3 Department of Urology, University of California, San Francisco, San Francisco,
CA 94143-0628.
Received July 28, 2003;
accepted after revision March 26, 2004.
Address correspondence to A. Qayyum.
Abstract
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MATERIALS AND METHODS. Endorectal MRI and MR spectroscopic imaging were performed in 43 patients with biopsy-proven prostate cancer before radical prostatectomy confirming organ-confined disease. For each sextant, two independent reviewers scored the degree of hemorrhage on a scale from 1 to 5 and recorded the presence or absence of capsular irregularity. A spectroscopist recorded the number of spectrally degraded voxels in the peripheral zone. The outcome variables of capsular irregularity and spectral degradation were correlated with the predictor variables of time from biopsy and degree of hemorrhage after biopsy.
RESULTS. Capsular irregularity was unrelated to time from biopsy or to degree of hemorrhage. Spectral degradation was inversely related to time from biopsy (p < 0.01); the mean percentage of degraded peripheral zone voxels was 18.5% within 8 weeks of biopsy compared with 7% after 8 weeks. Spectral degradation was unrelated to the degree of hemorrhage.
CONCLUSION. In organ-confined prostate cancer, capsular irregularity can be seen at any time after biopsy and is independent of the degree of hemorrhage, whereas spectral degradation is seen predominantly in the first 8 weeks after biopsy. MRI staging criteria and guidelines for scheduling studies after biopsy may require appropriate modification.
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Imaging Technique
MRI was performed on a 1.5-T whole-body MRI scanner (Signa, GE Healthcare).
The details of the MRI technique have been previously described
[16,
17]. Patients were examined
using the body coil for excitation and a pelvic phased-array coil in
combination with a commercially available balloon-covered expandable
endorectal coil for signal reception. Axial spin-echo T1-weighted images were
obtained from the aortic bifurcation to the symphysis pubis, using the
following parameters: TR/TE, 700/8; slice thickness, 5 mm; interslice gap, 1
mm; field of view, 24 cm; matrix, 256 x 192; frequency direction,
transverse (to prevent obscuration of pelvic nodes by motion artifact of the
endorectal coil); and 1 excitation. Thin-section high-spatial-resolution axial
and coronal T2-weighted fast spin-echo images of the prostate and seminal
vesicles were obtained using the following parameters: TR/TEeff,
5,000/96; echo-train length, 16; slice thickness, 3 mm; interslice gap, 0 mm;
field of view, 14 cm; matrix, 256 x 192; frequency direction,
anteroposterior (to prevent obscuration of the prostate by motion artifact of
the endorectal coil); and 3 excitations. All MR images were routinely
postprocessed to compensate for the reception profile of the endorectal and
pelvic phased-array coils
[18]. After review of the
axial T2-weighted images, a spectroscopic imaging volume was selected by an
experienced spectroscopist in conjunction with a technologist to maximize
coverage of the prostate, while minimizing inclusion of periprostatic fat and
rectal air. MR spectroscopic imaging of the peripheral zone is only routinely
performed because of limitations in gland coverage and the variable metabolic
spectra in the transition zone attributed to stromal and glandular hyperplasia
in benign prostatic hyperplasia
[16].
Three-dimensional MR spectroscopic imaging data were acquired using a water- and lipid-suppressed double spin-echo point-resolved spectroscopic imaging sequence optimized for the quantitative detection of both choline and citrate [16]. Water and lipid suppression was achieved using the band-selective inversion with a gradient dephasing technique [19]. Outer voxel saturation pulses were also used to improve volume selection, to eliminate contamination from periprostatic fat, and to reduce susceptibility problems due to the rectal air-tissue interface [20]. Data sets were acquired as 16 x 8 x 8 phase-encoded spectral arrays (1,024 voxels) with a nominal spectral resolution of 0.24-0.34 cm3 (TR/TE, 1,000/130; acquisition time, 17 min). The total examination time was 1 hr, including coil placement and patient positioning.
Image Interpretation
Two independent attending radiologists with subspecialty interest in
abdominal and prostate MRI and MR spectroscopic imaging retrospectively
reviewed the MR images of all 43 patients. Reviewers were aware that patients
had prostate cancer but were unaware of all other clinical and histopathologic
findings. In particular, reviewers were not aware that only patients with
organ-confined disease were included. The reviewers recorded the degree of
visible hemorrhage in the peripheral zone for each sextant on T1-weighted
images using a 5-point scale where 0 indicated no hemorrhage, 1 indicated
hemorrhage involving less than 25% of a sextant, 2 indicated hemorrhage
involving 25-49% of a sextant, 3 indicated hemorrhage involving 50-75% of a
sextant, and 4 indicated hemorrhage involving greater than 75% of a sextant.
In addition, the sum of the hemorrhage score in each sextant was used to give
a hemorrhage score for each patient. A total hemorrhage score was then
obtained for each patient by combining the scores for both reviewers.
On T2-weighted images, both reviewers documented the presence or absence of capsular irregularity, loss of the rectoprostatic angle, and neurovascular bundle involvement for each sextant and also recorded the presence or absence of seminal vesicle invasion [5]. Capsular irregularity was defined as spiculated or streaky low signal intensity extending from the capsule (Figs. 1A and 1B), low signal intensity in the periprostatic tissue, or focal irregular bulging of the capsule.
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The MR spectroscopic imaging data were overlaid on the corresponding axial T2-weighted images and evaluated by an experienced spectroscopist to determine those voxels in the peripheral zone that were unsuitable for analysis because of spectral degradation. Two spectral changes were associated with hemorrhage: The first was defined as a reduction in citrate but not choline and creatine because most of the citrate is in the ducts in which the blood collects. The second was an overall loss of all metabolites due to both a reduction in cell density and the blood occupying part or all of the spectroscopic voxel and spectral line broadening due to the presence of deoxyhemoglobin. Voxels were considered spectrally degraded by hemorrhage if they did not contain detectable peaks (peak area-to-noise ratio, > 5:1) for the prostatic metabolites (choline, creatine, and citrate) (Fig. 2) or if the voxels contained broad metabolite peaks (waterline width, > 20 Hz) in the regions of T1-weighted artifact. The number of voxels with degraded spectra and the total number of voxels in the peripheral zone were recorded for each patient.
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Lipid contamination and motion artifact may also result in spectral degradation but are associated with distinctive features (Fig. 3). Large lipid peaks are a feature of spectral degradation due to periprostatic lipid contamination. Broad water- and metabolite-line widths throughout the 3D MR spectroscopic imaging data set are features of spectral degradation due to motion artifact.
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Statistical Analysis
All statistical analysis was performed using SAS software version 8.2 (SAS
Institute). A p value of less than 0.05 was considered statistically
significant. We assessed interobserver agreement of reviews on the basis of
sextant results. Kappa statistics were calculated using generalized estimation
equations to adjust for the correlation among sextants from the same subjects.
Spearman's rank correlation was used for ordinal hemorrhage scores for each
sextant. The analysis of MRI results was based on a per-sextant analysis
(i.e., the outcome variable of per-sextant capsular irregularity was
correlated with the predictor variables of time from biopsy and degree of
per-sextant postbiopsy hemorrhage using a linear regression analysis). The
analysis of MR spectroscopic imaging results was based on a per-prostate
analysis (i.e., the outcome variable of percentage voxels with degraded
spectra in the peripheral zone was correlated with the predictor variables of
time from biopsy and degree of hemorrhage [total hemorrhage in peripheral
zone] using Spearman's rank correlation and Wilcoxon's rank sum tests,
respectively). Per-voxel or per-sextant analysis of hemorrhage score with MR
spectroscopic imaging was not performed because of the limitation of
misregistration of the spectroscopic voxels with T1- and T2-weighted images.
The MR spectroscopic data were not obtained from identical levels to T1- and
T2-weighted images and were subject to partial volume averaging effect from
adjacent tissue; therefore, we correlated total peripheral zone hemorrhage
with the total percentage of degraded spectra in the entire peripheral
zone.
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The two reviewers identified capsular irregularity in 36 (14%) and 30 (12%)
of 258 sextants, respectively (
= 0.45). Reviewers did not identify
loss of rectoprostatic angle, neurovascular bundle enlargement, or seminal
vesicle invasion in any patient. The observation of capsular irregularity was
not related to the time from biopsy or degree of visible postbiopsy hemorrhage
in the sextant on T1-weighted images (p > 0.05).
Spectral degradation was inversely related to time from biopsy (p < 0.01) (Fig. 5); the mean percentage of degraded voxels was 18.5% in patients imaged within 8 weeks of biopsy compared with 7% in patients imaged more than 8 weeks after biopsy. Spectral degradation was not related to total hemorrhage score (p = 0.37) (Fig. 6).
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Spectral degradation was found to be unrelated to the presence of visible postbiopsy hemorrhage on T1-weighted images but was significantly more frequent within the first 8 weeks after transrectal biopsy. This finding suggests that although postbiopsy hemorrhage and spectral degradation can occur together, postbiopsy change other than visible hemorrhage on T1-weighted images may be responsible for spectral degradation. The presence of postbiopsy hemorrhage on T1-weighted images is considered important because of the potential to over- or underestimate tumor extent or stage on MRI and MR spectroscopic imaging [12]. The inverse correlation of time from biopsy with spectral degradation in our study suggests that an interval of 8 weeks between MRI and MR spectroscopic imaging may be beneficial, rather than the previously recommended interval of 3 weeks [2, 12-14]. Such an increase in postbiopsy interval for optimal MRI and MR spectroscopic imaging would need to be balanced against patient anxiety, although this interval is probably negligible in terms of the natural history of prostate cancer.
Limitations of our study include the use of a patient population with organ-confined disease, which prevents assessment of the capsule appearances in patients with local tumor extension. In addition, we did not localize tumor nodules in this study because our purpose was to determine whether prostate capsule irregularity occurs in patients with organ-confined prostate cancer and to determine the impact of biopsy interval rather than local tumor staging on MR spectroscopic imaging. In a study of patients imaged within and after 3 weeks of biopsy, White et al. [12] showed a reduction in reviewer accuracy in the presence of postbiopsy hemorrhage within 3 weeks of biopsy. MRI and MR spectroscopic imaging are not routinely performed before prostate biopsy in patients suspected of having prostate cancer for logistic and economic reasons, and we could not evaluate patients with MRI and MR spectroscopic imaging performed before transrectal biopsy to confirm that the capsular changes were unrelated to any biopsy trauma or to determine the number of degraded voxels occurring in patients without biopsy. However, spectral degradation was inversely related to time from biopsy suggesting a causal relationship. Prostate biopsies were performed with variable techniques at a number of institutions rather than using a single standard institutional approach; this practice reflects the usual patient-referral procedure for preoperative MRI and MR spectroscopic imaging. However, the lack of a temporal relationship between capsular findings and biopsy indicates that capsular irregularity may not be related to prostate biopsy, irrespective of the technique. Localization of exact biopsy sites on imaging was not possible because of the limitations of accurate documentation of biopsy position inherent in the transrectal sonographic technique. Correlation of capsular irregularity on imaging with biopsy location and histopathologic findings is also difficult because they are not contemporaneous. Some overlap between hemorrhage grade and sextant localization is likely to have occurred because these observations are qualitative by nature, although the total number of abnormal sextants should not be affected.
In conclusion, in patients with organ-confined prostate cancer, capsular irregularity can be seen at any time after biopsy and is independent of the degree of hemorrhage, whereas spectral degradation is seen predominantly in the first 8 weeks after biopsy. MRI staging criteria and guidelines for scheduling studies after biopsy may require appropriate modification.
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