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1
Service de Radiologie, Hôpital Necker, 149 rue
de Sèvres, 75015 Paris, France.
2
Service d'Urologie, Hôpital Cochin, 24 Rue du
Faubourg saint Jacques, 75014 Paris, France.
3
Service d'Urologie, Hôpital Necker, 75015
Paris, France.
4
Service d'Uro-Gynécologie,
Hôpital Notre Dame de Bon Secours, 14 rue des
volontaires, 75014 Paris, France.
Received January 31, 2000;
accepted after revision March 7, 2000.
Address correspondence to F. Cornud, 15 Ave. Robert Schuman, 75007 Paris,
France.
Abstract
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MATERIALS AND METHODS. Ninety-four patients with nonsuspicious findings on digital rectal examination and a mean prostate-specific antigen level of 16.3 ± 10 ng/mL (median, 13 ng/mL) underwent endorectal sonography, color Doppler sonography, sextant endorectal sonographically guided biopsy, and endorectal MR imaging before radical prostatectomy.
RESULTS. Tumors were visible in 48 cases and not visible in 46. The mean Gleason biopsy score, the frequency of tumors involving three sextants or more of the prostate gland at biopsies, and the frequency of stage pT3 tumors were significantly higher in patients with visible tumors (5.9 ± 0.9, 42%, and 37.5%) than in those with invisible tumors (5.4 ± 1.1, 17%, and 17%). The 42 hypervascular tumors were hypoechoic in every case and had a higher rate of Gleason tumor grades 4 and 5 at biopsy than did the 52 hypovascular tumors (33% versus 11.5%). Six hypovascular tumors (6/52, 11.5%, two visible) had an insignificant tumor volume. Established extraprostatic tumor spread was detected on MR imaging in six of 18 cases (sensitivity, 33%; specificity, 100%0, all of which had the following four features: hypervascularity, prostate-specific antigen level greater than 20 ng/mL, three or more sextants of the gland having positive findings at biopsy, and seminal vesicle invasion.
CONCLUSION. Endorectal sonography and color Doppler sonography are useful to differentiate low-risk invisible and hypovascular tumors from high-risk visible and hypervascular tumors. However, MR imaging has a poor sensitivity for the detection of extraprostatic spread and is accurate only in a minority of highly selected high-risk hypervascular tumors.
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Color Doppler sonography was performed by two experienced operators using a 7.5-MHz endview probe (Acuson, Mountain View, CA). Color flow imaging was adjusted to the low-flow program in every case (threshold of velocity detection, 2.3 cm/sec), and the color Doppler gain was set just below the color noise threshold. Vascularization of hypoechoic nodules of the peripheral zone was evaluated by comparison with vascularization of an adjacent or contralateral peripheral zone without using a grading system. A hypoechoic image (Fig. 1A,1B) or an area with a subtle decrease in echo structure (Fig. 2A,2B) was considered hypervascularized if it contained more vessels than the adjacent peripheral zone. Conversely, a hypoechoic nodule was defined as hypovascularized if the number of vessels was similar to or less than that in the adjacent peripheral zone (Fig. 3A,3B). Color Doppler imaging was also performed to detect areas of increased peripheral zone vascularization when endorectal sonography showed no gray-scale abnormality. Because benign prostatic hyperplasia has a heterogeneous pattern and commonly contains hyperplastic nodules, color Doppler sonography was not used to detect suspicious abnormalities originating in the transition zone.
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Sextant biopsies were performed endorectally with an 18-gauge needle
mounted on a spring-loaded biopsy device (Bard, Paris, France). Directed
biopsies comprised two passes into all hypoechoic areas visible on endorectal
sonography and any hypervascular area with no endorectal sonography gray-scale
abnormalities. Sextant biopsies included one ipsilateral pass into each
isoechoic sextant adjacent to any abnormal area, and one core was also taken
from each contralateral sextant midway between the midline and the lateral
aspect of the prostate. Each biopsy was specifically labeled as to its source
(right or left apex, mid portion, or base) to be sure that a specific biopsy
corresponded to a specific lesion. At least six to eight cores were taken, and
the number of sextants (of six) involved by the tumor was recorded. Tumors
involving fewer than three sextants (percentage of positive biopsies < 50%)
were compared with tumors invading at least three sextants (percentage of
positive biopsies 
50%)
[24]. In 36 patients with a
prostate weight of more than 40 g (estimated with the ellipsoid formula), four
to six deep biopsies of the anterior portion of the transition zone were also
performed: two near the apex, two near the prostate base, and two in the mid
portion of the transition zone. Cores were inked at their distal end to
identify anterior transition zone tissue.
Pathologic staging was done by three uropathologists (one in each of the three participating centers) according to a modified Stanford technique [26]. Surgical margins were not inked before sectioning. The prostate gland was fixed in 10% buffered formaldehyde. The seminal vesicles and apex were separated and examined on sagittal sections. The mid portion of the gland was sectioned axially at 5-mm intervals. The pT classification was used to assess intra- and extraprostatic tumor spread. The pathology report specified the location of the tumor in the prostate (apex, mid portion, or base) and was compared with the labeled biopsies and the endorectal sonograms to verify that hypoechoic lesions actually corresponded to the tumor on radical prostatectomy specimens. Although tumor volume was not routinely measured, a tumor was classified as insignificant when only a few tumor cells were found. Capsular penetration was classified as "focal" if a few tumor cells were present exterior to the prostate or as "established" if more extensive extraprostatic spread was present, according to the Epstein classification [25]. Seminal vesicle invasion was defined as minimal if only the intraprostatic portion of the vesicles was involved and as extensive if the extraprostatic portion of the vesicles was involved. Surgical margins were considered positive when the tumor showed histologic extension to the surface. In 14 patients (14.8%), a single positive margin (apical in eight patients and anterior or anterolateral in six patients) was observed in an area without periprostatic tissue, with no signs of capsular penetration; these tumors were classified as pT2 with a positive margin caused by inadvertent incision of the capsule during surgery [26].
Endorectal MR imaging was performed 2-3 weeks after biopsy, and none of the patients received androgen privation therapy during the interval. MR imaging analysis was conducted in consensus by two observers who had several years' experience in interpreting endorectal images and who were aware of the results of digital rectal examination, endorectal sonography, color Doppler imaging, sextant biopsies, and PSA level. Discrepancies occurred in 11.7% (11/94) of cases about signs of capsular penetration and were resolved by consensus with a third observer. We used a 1.5-T superconducting magnet (Signa; General Electric Medical Systems, Milwaukee, WI) and the endorectal surface coil (MedRad, Pittsburgh, PA) coupled to an anterior surface coil. After a gradient-echo localizer sequence to check coil position, fast spin-echo sequences were acquired (TR/TE, 3000/102 msec; section thickness, 4 mm; intersection gap, 0.4 mm; signals acquired, two; field of view, 16 cm; matrix, 512 x 256; and no phase wrap). Axial T1-weighted sequences were acquired to detect biopsy artifacts and to assess lymph node involvement. T2-weighted sequences were acquired in the axial and coronal planes, the latter focusing on the caudal junction of the vas deferens and seminal vesicles. Capsular penetration was diagnosed if MR imaging showed irregular bulging of the prostate associated with disruption of the capsular signal or periprostatic fat infiltration. The latter included a tumor signal within periprostatic fat (Figs. 4A and 4B), obliteration of the rectoprostatic angle (Figs. 5A and 5B), or asymmetry of the neurovascular bundles (Fig. 6). Indirect signs such as smooth bulging or broad tumor contact were not included. Seminal vesicle invasion was diagnosed when a focal hyposignal was present in one or both seminal vesicles; focal thickening of the tubular walls (Fig. 7A,7B) on T2-weighted sequences was considered evidence of seminal vesicle invasion [27] only if the prostate base was at least unilaterally involved by the tumor on biopsies.
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Prostatectomy Specimens
Table 3 presents the results
of examinations of specimens from radical prostatectomy of visible, invisible,
hypervascular, and hypovascular tumors in 94 patients with nonpalpable
prostatic cancer.
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Insignificant cancer.—Six patients with positive findings on a single biopsy with tumor length shorter than 3 mm had an insignificant tumor volume; volume was limited to a few tumor cells in four patients, and no cancer cells were detected in two patients. The six tumors were hypovascular, and two of these patients had a hypoechoic hypovascular nodule at the positive biopsy site. No patient with a hypervascular cancer had an insignificant tumor.
Gleason score and pT stage.—The mean Gleason score (6.3 ± 1), rate of Gleason score 4 or 5 (18/48, 37.5%), and rate of stage pT3 tumors (18/48, 37.5%) were significantly greater in patients with visible tumors than in those with invisible tumors (5.6 ± 1, p < 0.001; 6/46, 13%, p < 0.001; and 8/46, 17%, p < 0.001, respectively). Seminal vesicle invasion was more frequent in visible tumors (12/48, 25%) than in invisible tumors (4/46, 9%). Comparable significant differences were observed between hypervascular and hypovascular tumors (Table 3).
Endorectal MR Imaging
Capsular penetration.—At pathologic examination, capsular
penetration was present in 22 patients. Penetration was focal in 16 patients,
of which MR imaging detected none (sensitivity, 0%), and established in six
patients, of which MR imaging detected four (sensitivity, 67%).
Seminal vesicle invasion was present in 16 cases. It was minimal in eight patients, of which MR imaging detected none. It was extensive in eight patients, of which MR imaging detected four (sensitivity, 50%). MR imaging showed seminal vesicle wall thickening in two of these patients in which at least one biopsy showed positive findings in the prostate base. Wall thickening was observed in another four patients who had no positive findings at biopsy of the prostate base. These patients were considered to have no seminal vesicle invasion, and pathologic examination revealed stage pT2 tumors. In one of four patients with undetected seminal vesicle invasion, MR imaging showed small hypotrophic hypointense seminal vesicles that were considered nonspecific in a patient with positive findings at one biopsy of the prostate base.
MR imaging accuracy for stage pT3 detection.—Overall, 26
tumors (27.6%) were stage pT3. Extraprostatic spread was established in 18
patients, of which MR imaging detected six (sensitivity, 30%). Extraprostatic
spread was focal in eight patients but was not detected in any. No
false-positive diagnoses of extraprostatic spread were made (specificity,
100%), giving an overall accuracy of 78%, with positive and negative
predictive values of 100% and 86%, respectively. The characteristics of stage
pT3 tumors detected on MR imaging are shown in
Table 4. MR imaging detected
extraprostatic spread only in men with hypervascularized tumors and the
highest risk factors on biopsy specimens (mean Gleason score, 6.6 ±
0.5; high Gleason scores in 67% [4/6] of patients; percentage of tumors with
positive findings on biopsy 50% in every patient). In addition, the PSA
level was greater than 20 ng/mL and seminal vesicles were invaded on the
prostatectomy specimen in every patient.
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The ability to distinguish visible from invisible nonpalpable prostate cancer has prognostic consequences. Although two studies [2, 3] showed no significant differences between the two types of tumor with regard to tumor volume, the Gleason score, or pathologic stage, Ohori et al. [1] reported that visible nonpalpable tumors were more likely to extend outside the prostate than were invisible tumors (47% versus 18%). Our results are similar: we found that stage pT3 tumors were more frequent in men with visible tumors, as expected from their higher Gleason score and their greater percentage of tumors with positive biopsy findings equal to or exceeding 50%. Color Doppler sonography added only minor information because most of the differences between hypervascular and hypovascular tumors were similar to those between visible and invisible tumors. However, color Doppler sonography was superior to endorectal sonography in two circumstances. The first, previously reported by others [9, 11], is the significantly greater rate of high Gleason grades in hypervascular cancerous tumors. This difference could not be seen on biopsy results if the gray-scale classification alone was used, and this finding supports the usefulness of targeting hypervascular lesions or portions thereof [11] to improve the detection rate of tumors with a high Gleason grade. The second circumstance is the dilemma created by positive findings on a single biopsy with a tumor length shorter than 3 mm, which was better resolved on color Doppler sonography in our study. These microfoci still raise the possibility of an insignificant tumor that might not require aggressive treatment [5]. However, such was never the case in patients with hypervascular tumors because all the insignificant tumors in our series were hypovascular. Color Doppler sonography is thus a good additional examination to rule out, on an individual basis, insignificant tumor volume in patients with hypervascular cancer and a single microfocus on biopsy.
Preoperative local staging would be advisable for patients with visible and hypervascular tumors. These patients are at a high risk of extraprostatic spread; we found 43% of stage pT3 tumors, a rate similar to that of extraprostatic spread of palpable T2 cancers [1]. Endorectal MR imaging is the only imaging technique that can achieve this goal, with a current specificity of 90-95% [22], thanks to technical refinements (the routine use of fast spin-echo sequences, anterior coil coupling) and standardization of criteria for interpreting MR images (experienced observers [14], discarding indirect signs [18, 19], and using only direct signs of established seminal vesicles [17, 20]). Specificity of 100% has rarely been achieved and then only by individual radiologists, as reported by Tempany et al. [21]. However, because nonpalpable tumors have little if any bulging of the posterior or lateral prostate contours, the most common misleading MR sign of extraprostatic spread (irregular bulging of the prostate contour [19, 37]), is avoided. Likewise, to avoid the false-positive diagnosis of seminal vesicle invasion, focal thickening of the wall of the seminal vesicle, a nonspecific sign [38], was interpreted as evidence of seminal vesicle invasion only if at least one biopsy had positive findings in the prostate base, because the probability of seminal vesicle invasion is negligible in the absence of positive findings at prostate base biopsy [39].
Unfortunately, this high specificity is offset by poor sensitivity. In our series, MR imaging detected occult established extraprostatic spread in only 30% of men with visible and hypervascular tumors and never detected stage T3 in true stage T1c tumors. This poor sensitivity is a major limitation of the use of MR imaging for staging, even in cases of hypervascular tumors. Our study showed that hypervascularity was not a sufficient criterion for referring patients for MR imaging because MR imaging is accurate in only a minority of high-risk patients defined not only by the presence of a hypervascular tumor but also by a PSA level greater than 20 ng/mL and at least half the prostate involved by the tumor on endorectal sonographically guided biopsies.
In conclusion, endorectal sonography and color Doppler sonography can differentiate low-risk nonpalpable prostate tumors, which are hypovascular (and invisible in 90% of cases), from high-risk carcinoma (subclinical T2 stage), which is visible and hypervascular. However, MR imaging has a sensitivity of only 30% for detecting extraprostatic spread and is accurate in only a minority of patients with the highest risk of extraprostatic spread, which cannot be defined by hypervascularity alone on color Doppler sonography; extraprostatic spread is also defined by the PSA level and the percentage of biopsies with positive findings.
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