Are extended biopsies really necessary to improve prostate cancer detection?

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1 (2003) 6, & 2003 Nature Publishing Group All rights reserved /03 $ Are extended biopsies really necessary to improve prostate cancer detection? R Damiano*,1, R Autorino 3, S. Perdonà 3, M. De Sio 3, A Oliva 1, C Esposito 2, F Cantiello 1, G Di Lorenzo 4, R Sacco 1 & M D Armiento 3 1 Urologic Clinic, Magna Graecia University of Catanzaro, Italy; 2 Department of Clinical and Experimental Medicine, Magna Graecia University of Catanzaro, Italy; 3 Urologic Clinic, Second University of Naples, Italy; and 4 Department of Oncology, Federico II University of Naples, Italy The aim of this study is to understand the value of specific sites in extended peripheral and transition zone biopsy schemes in order to define the optimal systematic biopsy regimen correlated with the percentage of positivity of each single bioptic site. A total of 165 consecutive patients underwent transrectal ultrasonography examination to detect prostate cancer followed by a lesiondirected and systematic 14-step biopsy scheme. The detection rate was examined for the lesion-directed and for each zone region biopsy. The frequency of positive biopsies in the various prostate regions was determined to evaluate the diagnostic yield of each biopsy site. Analysis was stratified for prostate-specific antigen (PSA), free-to-total PSA ratio, age, prostate size and digital rectal examination. The biopsy protocol detected 40% of patients (66/165) as positive and 55.1% (91/165) as negative for cancer. Standard sextant biopsy was expected to detect only 51 cancer on 66, lateral peripheral (PZ), transition (TZ) and central zone (CZ) biopsies only 56 cancer on 66, while the combination of sextant, PZ, TZ and CZ biopsies, for a total of 14 zone biopsies, detected 64 on 66 patients with cancer (97%) at recruitment. Sampling only the eight prostate regions with higher frequency of positive cancer biopsy was expected to detect 61 cancer patients against the 64 found with the 14-step scheme. This eight-biopsy regimen outperforms the conventional sextant regimen in cancer detection rate (93 vs 77%) and has an overall detection rate lower by only 3.1% (36.9 vs 40%) compared to the 14-biopsy regimen. This difference in detection rate is even smaller in patients with PSA values o10 ng/ml, age o70 y and prostate size o50 ml. This eight-biopsy scheme, including sampling in PZ and TZ toward the base, should be considered in an initial biopsy scheme to maintain a similar detection rate of an extensive biopsy scheme reducing the number of biopsies. (2003) 6, doi: /sj.pcan Keywords: biopsy; prostatic neoplasm; prostate-specific antigen Introduction *Correspondence: Rocco Damiano, Magna Graecia University of Catanzaro, Via T Campanella 202, Catanzaro, Italy. damiano@unicz.it Received 26 February 2003; revised 20 May 2003; accepted 21 May 2003 The systematic parasagittal sextant biopsy technique under transrectal ultrasound (TRUS) guidance has been introduced in 1989, showing to be superior to lesiondirected biopsies in detecting prostate cancer. 1 Since then, the sextant method has become accepted as the gold standard biopsy technique, even if it could be suboptimal due to a positive detection rate as low as 20 30%. 2,3 Furthermore, 20 40% of patients with persistently elevated prostate-specific antigen (PSA) have a positive repeat biopsy, suggesting that many patients with prostate cancer initially remain undiagnosed with the sextant technique. 4,5 Moreover, since the majority of prostate cancers originate from the peripheral zone (PZ), sextant biopsies

2 may be inadequate. Alternative biopsy strategies have been suggested, with increased number of systematic biopsies, sampling the lateral aspect of the PZ and/or transitional zone (TZ) and modifying the biopsy angle to better assess the PZ, and increasing biopsy core length to attempt a more reliable prostate cancer detection. Stamey 6 suggested that the TZ and lateral PZ should be included in the sextant strategy, while Eskew et al 7 reported a biopsy scheme that samples five regions, the lateral aspect of the PZ, the conventional sextant zone for each side and the midline prostate zone. He could observe, in a prospective study, an increased detection rate compared to the sextant method and recommended an increased number of biopsies. More recently, Durkan et al 8 found that an extended-core biopsy protocol significantly improves the detection rate for prostate cancer and routine TZ biopsies should be considered for men with serum PSA levels of 10 ng/ml. We have evaluated the efficacy of specific sites in an extended PZ and TZ biopsy scheme in order to define an optimal systematic biopsy regimen correlated with a higher percentage of positivity of each single bioptic site. Conventional sextant biopsies Midlobar parasaggittal plane at apex, midgland and base Lateral biopsies Peripheral zone lateral border at midgland (anterior horn-) Medial biopsies Transition zone toward base and apex Central biopsies Midline central zone (ML) BASE TZ ML TZ BASE 14 step biopsy scheme 251 Patients and methods Between January 1999 and February 2001, 165 consecutive patients (mean age y), referred for abnormal screening digital rectal examination (DRE) and/or PSA level 44 ng/ml, gave their informed consent to undergo TRUS examination followed by lesion-directed and systematic biopsies to detect prostate cancer. All the biopsies were performed by a urologist specifically trained to use an ultrasound Kretz s unit with an endocavitary multiplanar probe. Prostate size was evaluated by computer ultrasound software using the specific ellipsoid formula (0.52 length width height). Biopsies were performed with a spring-loaded automatic biopsy device using an 18-gauge 22 mm core Tru-Cut s needle. All patients underwent a 14-step biopsy scheme and, if necessary, direct lesion biopsies. Thus, the various regions of the prostate were sampled in a similar manner in all 165 patients (Figure 1). Any clear hypoechoic lesions outside the biopsy scheme site were detected and sampled before systematic biopsies. No patient required sedation and each received five doses of 500 mg ciprofloxacin the day before, on the morning of and 3 days after biopsy, and a fleet enema 2 h before biopsy. None of the patients had previously undergone prostate biopsy, so all were primary procedures at recruitment. Conventional sextant biopsies were obtained in the midlobar parasagittal plane (halfway between the lateral edge and the midline of the prostate gland) at the apex, midgland and base. Lateral biopsies were performed just medial to the lateral border of the prostate at the midgland. The right and left lateral midgland sites, also definied as anterior horn (), represent the extreme lateral and anterior aspect of PZ tissue that surrounds the TZ, and are obtained in the sagittal plane identifying the most lateral PZ of prostate tissue. Two medial biopsies for each side were obtained in the paraurethral zone, specifically in the TZ toward the base and apex and one for each side in the central zone (CZ). All biopsy cores Figure 1 Conventional sextant biopsies Midlobar parasaggittal plane at apex and midgland Lateral biopsies Peripheral zone lateral border at midgland (anterior horn-) Medial biopsies Transition zone toward base TZ 8 step biopsy scheme were labelled and submitted separately to be examined by the same pathologist. The detection rate was examined for the lesion directed and for each zone region biopsy (apex, midgland and base at sextant plane, lateral PZ at midgland, TZ medially toward the base and apex and CZ of the gland). The frequency of positive biopsies in the various prostate regions was determined to evaluate the diagnostic yield of each biopsy site. Cancer detection rates between different biopsy schemes were compared using McNemar s test. Analysis was stratified for PSA, free-to-total (F/T) PSA ratio, age, prostate size and DRE. Complications between different age groups were compared using the Mann Whitney U-test. A statistics software was used and a P-value o0.05 was considered significant. In case of negative results on biopsy, the procedure was repeated at 1 y in case of persistently elevated PSA Biopsy scheme showing 14- and 8-core strategy.

3 252 or increased velocity or suspicious F/T PSA ratio, while it was repeated at 3 months in the case of a suspicious lesion on biopsy. Suspicious lesions were represented by atypical small acinar proliferation with atypical cytological and architectural features incompatible with a diagnosis of prostate cancer, and high-grade prostate intraepithelial neoplasia (PIN). Table 1 Results of biopsies according to clinical and PSA indications Pts Indications Cancer Detection rate (%) 61 (37%) DRE+ PSA > (17%) DRE+ PSAo (46%) DRE PSA > Results The biopsy was positive for cancer in 66/165 (40%) and negative in 91 (55.1%). The overall mean (s.d.) prostate volume was ml for the entire population and ml for cancer patients; the median (s.d.) age was y for the entire population and y for the cancer-positive group. Indications for and results of biopsies are summarized in Table 1. Serum PSA was significantly higher in the 66 (40%) patients with prostate carcinoma (mean 11.3 ng/ml) than in 91 without prostate cancer (mean 4.3 ng/ml). Among the 76 patients with only PSA 44 and normal DRE, we detected 21 cases of cancer, that is, about 28% of cases. Eight (4.8%) patients presented suspicious lesion at biopsy, four of them with high-grade PIN and four with atypical cell. Repeat biopsy at a 3-month follow-up revealed cancer in all cases. Follow-up of negative cases lasted 37 months (mean value, range months). A PSA velocity ng/ml/y has been seen in five out of 91 patients (5.5% of negative cases). Among these five patients, negative at first biopsy, and submitted to repeat biopsy at a 1-y interval, three presented cancer, one high-grade PIN and another presented atypical cells. Re-biopsy of these latter two cases at 3 months revealed cancer in both. Out of 91 patients, 13 (14.3% of the negative cases) had persistently elevated PSA or suspicious F/T PSA ratio at a 12-month follow-up, but at repeat biopsy only one presented cancer, while one, who was lost to follow-up, presented high-grade PIN. Follow-up showed all but six (93.4%) patients with negative biopsy to remain negative, while, at a median follow-up of 37 months, 73 negative patients (80.2%) experienced no variation in PSA velocity in two samples/y, no change in DRE, no persistently elevated PSA level and abnormal F/T PSA ratio. Out of a group of 165 patients at a mean follow-up of 37 months, we detected 66 cancers on recruitment, and missed six cancers that had been negative at the first biopsy (re-biopsy detection time range 6 22 months). Regarding the group with suspected cancer, after repeating biopsy at a 3-month interval, we detected eight more cases. Prostate cancer was detected with lesion-directed biopsies and a 14-step biopsy scheme in 66/165 men (40%). Standard sextant biopsies were expected to detect only 51 on 66 patients with cancer (77%), while PZ, TZ and CZ biopsies were expected to detect only 56 patients with cancers (85%). The combination of all of them, for a total of 14 zone biopsies, detected 64/66 cases (97%) at recruitment. Further two cases were detected in two patients with hypoechoic lesions suggestive of cancer Table 2 Site Positive core biopsies and frequencies by prostate regions Negative biopsy cores (n=749) Positive biopsy cores (n=175) Average positive frequency Left Sextant base Sextant med Sextant apex Tz medial base Lat midgland Tz medial apex Central zone Right Sextant base Sextant med Sextant apex Tz medial base Lat midgland Tz medial apex Central zone Three positive biopsy cores in hypoechoic regions outside the bioptic scheme. located outside the extended biopsy scheme. Overall, this extensive protocol compared to the standard sextant regimen resulted in a 9.1% improvement in the detection rate in the entire group of 165 patients. PZ, TZ and CZ biopsies detected 13 cases of cancer among 66 with negative sextant biopsies. As to the localizations, there were seven cancers on PZ biopsies (four on the right and three on the left lateral midgland site), four on TZ biopsies (one toward the apex on the right and three toward the prostate base, two on the right, one on the left) and two on the CZ of the prostate. Out of 927 bioptic samples from the prostate cancer patients group, 178 were positive for cancer in 66 patients, with mean sample value for cancer patient of 2.7. The average positive frequency rate was 14.8% of samples for sextant sites (59/396), 21.9% for PZ, TZ and CZ sites (116/528) and 18.9% for the extended 14-step scheme (175/924) (Table 2). The majority of the cancers detected were considered significant. Only 14 patients presented a single positive bioptic core (21.5%) and among them only three presented with a Gleason score sum of 5 or less, only one having a needle length involvement less than 3 mm. The frequency of patients with positive biopsy (66 on 165) and the frequency of positive cancer biopsies (178/ 927 from 66 cancer patients) from each prostate region allowed us to identify the prostate zone regions with a higher frequency of positivity for cancer and thus to create a new biopsy strategy, compare the variations in

4 cancer detection rate with different schemes and eliminate biopsy sites from the systematic 14-biopsy regimen. Of the 14 systematic zone regions, the CZ, the sextant midlobar base and TZ toward the apex resulted in the lowest cancer detection rates, while the most effective biopsy sites were the, the sextant apex, the TZ paraurethrally toward the base of the prostate and the sextant midlolbar midgland, which proved to be the configuration with overall better results. Analyzing only cores from these areas, we expected to detect 61 cancer patients (93%) against 64 (97%) with the 14-step scheme, and 134 cancer biopsy samples out of 175 (76.5%) thus maintaining the same specificity obtained with the biopsy regimen. Routine sextant biopsies were expected to detect cancer in 51/66 patients (77%) of the cancer group and in 59/175 positive core samples. An increase in 75 positive cores (from 59 to 134) out of 175 samples in cancer detection rates was observed considering an eight-step regimen for the standard systematic sextant biopsy scheme, while an increase by 116 in 175 samples in the biopsy sample detection rate was observed when the biopsy technique included all 14 areas. Overall, the difference in the entire group of 165 patients between an extensive protocol with 14 biopsies and eight-step protocol was 3.1%. We therefore analyzed the frequency of cancer patients on biopsy in relationship to PSA level, PSA F/T ratio (greater than 20% and smaller values) in the PSA range 4 10 ng/ml, age (below 70 y and older ones), prostate volume (greater than 50 ml and smaller ones) and DRE. The analysis (Table 3) showed that the differences between the 14- and the eight-step scheme were smaller in men with PSA 10 ng/ml or less (2.9%) and F/T ratio o0.2 (0%), age o70 y (1.1%), size o50 ml (1.7%) and negative DRE (2.6%) than in those with PSA greater than 10 ng/ml (5.2%). In our group of patients, applying the eight-step biopsy scheme, we report a cancer detection rate of 39.8% (45/113) in patients in whom prostate volume was less than 50 ml compared with 30.8% (16/52) in those with a volume exceeding 50 ml. A similar difference rate was not detected when comparing prostate volumes more or less then 50 ml with the standard sextant biopsy scheme and was less evident with the extended 14-step protocol. During the follow-up of negative cases, we detected further six patients with cancer, who underwent rebiopsy because of persistently elevated PSA and/or Table 4 Complications (%) suspicious F/T PSA level in one and with increasing PSA level in five. Sites of positive biopsy samples were the lateral midgland left and/or right in 4/6 patients, the TZ toward the base in 3/6 and the TZ toward the apex out of the 8 step scheme in only one. The incidence of morbidity in this biopsy protocol was low. In patients who underwent a 14-step biopsy regimen, main and immediate complications (Table 4) were discomfort on examination, referred by 35.7% (59/165) of patients, slight and gross hematuria in 33.3% (55/165), moderate to severe vasovagal episodes in 4.8% (8/165), and chills and fever in 3.6% (6/165). Acute urinary retention developed in 5.4% (9/165), and in all cases the catheter was removed within 7 days. Fever and or infectious complications were noted as a result of the procedure in three patients. Overall, older patients tolerated the procedure with less discomfort than younger patients. Discussion Complications of 14step scheme biopsies of the prostate Age o70 y (n=103) Age >70 y (n=62) P-value Rectal bleeding 9 (8.7) 4 (6.4) 0.69 Gross hematuria 15 (14.5) 7 (11.2) 0.67 Slight hematuria 21 (20.3) 12 (19.3) 0.59 Vasovagal episodes 4 (3.9) 4 (6.4) 0.93 Chills and fever 3 (2.9) 3 (4.8) 0.36 Acute retention 5 (4.8) 4 (6.4) 0.67 Fever > (1) 2 (3.2) 0.71 Discomfort on exam 27 (26.2) 32 (51.6) 0.05 Biopsy technique under TRUS guidance has emerged as the preferred method and is widely used for detecting prostate cancer. Since most cancers originate in peripheral areas, not sampled by the standard systematic sextant biopsy strategy, it is logical that more laterally directed biopsies may have an improved diagnostic yield compared to standard sextant samples. Chen et al 9 used a stochastic computer simulation model of ultrasoundguided biopsies with mathematically reconstructed radical prostatectomy specimens and analyzed the effectiveness of sextant biopsies, which are widely 253 Table 3 Overall and stratified results among different biopsy schemes Pts Standard sextant Extensive protocol Eight-step protocol Diff % 8/14 Overall (30.9%) 66 (40%) 61 (36.9%) 3.1 P=0.42 PSAo (32.3%) 28 (41.1%) 26 (38.2%) 2.9 P=0.81 PSA F/T o (33.3%) 13 (43.3%) 13 (43.3%) 0 P=0.95 PSA F/T > (31.5%) 15 (39.4%) 13 (34.2%) 5.2 P=0.92 PSA > (29.9%) 32 (32.9%) 37 (38.1%) 5.2 P=0.71 Age o (31.8%) 35 (39.7%) 34 (38.6%) 1.1 P=0.63 Age > (29.8%) 31 (40.2%) 27 (35.0%) 5.2 P=0.76 Size o (30.9%) 47 (41.5%) 45 (39.8%) 1.7 P=0.64 Size > (30.7%) 19 (36.5%) 16 (30.8%) 5.8 P=0.91 DRE (30.3%) 37 (41.5%) 34 (38.2%) 3.3 P=0.62 DRE (31.5%) 29 (38.1%) 27 (35.5%) 2.6 P=0.97

5 254 adopted in clinical practice. He was able to detect cancer reliably in only 73% of patients in whom the total tumor volume was greater than 0.5 cm 3. The addition of biopsy of the anterior TZ, midline PZ and inferior portion of the of the PZ reliably detected cancer in 96% of patients with total tumor volume greater than 0.5 cm 3. Results from Bauer et al 10 using biopsy simulation of threedimensional (D) reconstructed whole mount radical prostatectomy specimens showed that the highest cancer probability areas were the far lateral crescent-shaped areas of the PZ from the apex to the midgland. The current literature describes a trend toward increasing number of cores obtained and the sites biopsied from more lateral regions of the gland beyond those of the standard sextant technique. 11 The reasons for the most effective biopsy sites can be explained by prostate anatomy: most prostate cancers originate from PZ, and at midgland the PZ shows an anterior lateral horn (), so lateral biopsies at midgland lie completely in the PZ. At the prostate apex, only the PZ exists and only apical biopsies sample this zone. Our data confirmed this assumption by showing, with an extended biopsy scheme including 14 biopsies and lesion-directed biopsy at the initial TRUS, an improvement in cancer detection up to 40%, missing only six patients with cancer on 165 at a 37-month follow-up. Using this strategy we demonstrated that the likelihood of finding prostate cancer in men with a normal DRE and serum PSA 44 was 28%, which is quite similar to the 25% rate reported in a study by Keetch et al. 4 We therefore reported all patients with suspicious lesion at initial biopsy presenting cancer at re-biopsy with a 14-step extended biopsy scheme. Overall, the reported incidence of atypia is between 1.5 and 5% 12,13 and 2 and 16% for high-grade PIN. 14 The reported incidence of prostate adenocarcinoma in patients with previous detected suspicious lesions in several studies ranged between 27 and 79% for highgrade PIN and 29 and 60% for atypia, 15 while the largest comparable study to our knowledge reports a cancer detection rate of 40% for the atypia group and 23% for the high-grade PIN group on initial biopsy. 16 In our group, we did not detect any associated cases of atypia and high-grade PIN. PSA velocity resulted in a good predictor of prostate cancer. 17 In our series, during a mean follow-up of 37 months, the increase of PSA velocity by more than 0.75 ng/ml for a 1-y interval in patients who had previously undergone extended biopsy was correlated with cancer in three patients of five after a first set of re-biopsy and in further two of two after the second set 3 months later. The 14-core multisided directed biopsy strategy, previously used and retrospectively analyzed, in the manner described was tolerated by patients even without sedation. In our study, of the different zone regions, the PZ lateral border at midgland (), the apex and the midlobar base of the sextant strategy and TZ toward the base presented higher frequencies of positivity. Overall cancer detection rate, analyzing only cores from the biopsy sites of this novel eight-step scheme, was 36.9% and maintains a similar detection rate (93 vs 97%) in the 14-step regimen and a higher difference compared to standard sextant regimen, allowing one to detect more sample cancers (93 vs 77%) than the standard sextant regimen. The difference in detection rate between 14- and 8- scheme biopsy is less evident, although not to a statistically significant extent, with PSA value o10 ng/ ml, age o70 y, prostate size o50 ml and normal DRE. Comparing the detection rate using the standard sextant biopsy technique, we do not detect wide differences for different PSA values, age group, prostate size and DRE characteristics, while other authors have reported lower cancer detection rates with increasing prostate volume using the standard sextant biopsy technique. 18,19 The reason for different results in our series should be related to the lower overall mean prostate volume of the entire population and cancer group compared to other presented papers. We do not currently suggest CZ biopsy as the standard procedure for first-time prostate biopsy, as this produces severe discomfort to the patient and, because of the invasiveness of the procedure on the urethra, it is associated with a high incidence of bleeding, as reported by Eskrew et al. 7 Moreover, prostate cancers arising from CZ represent less than 8% of cases, as described first by Mc Neal et al, 20 and biopsy in this region should improve cancer detection only in patients who are undergoing repeat biopsy for persistent adverse clinical parameters. Prophylactic antibiotics given before the biopsy procedure help prevent severe clinical complications. As reported in a study by Lindert, 21 this is true even if they are given after the biopsy procedure. While we do not recommend this approach, the effectiveness of postbiopsy dosing is reassuring if a patient without complications fails to receive the prescribed dose before the procedure. Conclusions The extended biopsy scheme has consistently decreased the false-negative rate of the sextant biopsy by taking additional samples, but the yield of each single bioptic side result is so widely different to allow the elimination of samples from specific prostate zone sites. This eightstep novel scheme, maintaining a similar detection rate of a 14-step extended biopsy scheme, especially in younger patients (age o70 y), with PSA value o10 ng/ ml and prostate size less than 50 ml, while reducing the number of biopsies, should be considered as an initial biopsy scheme for use in an outpatient program. A larger number of patients and a multicenter study are warranted to test our initial results. References 1 Hodge KK, Mc Neal JE, Terris MK, Stamey TA. Random systematic versus directed ultrasound guided transrectal core biopsies of the prostate. JUrol1989; 142: Flanigan RC et al. Accuracy of digital rectal examination and transrectal ultrasonography in localizing prostate cancer. JUrol 1994; 152: Naughton CK et al. Clinical and pathologic tumor characteristics of prostate cancer as a function of the number of biopsy cores: a retrospective study. Urology 1998; 52:

6 4 Keetch DW, Catalona WJ, Smith DS. Serial prostatic biopsies in men with persistently elevated serum prostate specific antigen values. JUrol1994; 151: Ellis WJ, Brawer MK. Repeat prostate needle biopsy: who needs it?. JUrol1995; 153: Stamey TA. Making the most out of six systematic sextant biopsies. Urology 1995; 45: Eskew LA, Bare RL, McCullough DL. Systematic 5 region prostate biopsy strategy is superior to sextant method for diagnosing carcinoma of the prostate. J Urol 1997; 157: Durkan GC et al. Improving prostate cancer detection with an extended-core transrectal ultrasonography-guided prostate biopsy protocol. BJU Int 2002; 89: Chen ME et al. Comparison of prostate biopsy schemes by computer simulation. Urology 1999; 53: Bauer JJ et al. Three dimensional computer-simulated prostate models: lateral prostate biopsies increase the detection rate of prostate cancer. Urology 1999; 53: Matlaga BR, Eskew LA, Mc Cullogh DL. Prostate biopsy: indications and technique. JUrol2003; 169: Cheville JC, Reznicek MJ, Bostwick DG. The focus of atypical glands, suspicious for malignancy in prostatic needle specimens. Incidence, histologic features, and clinical follow-up of cases diagnosed in a community practice. Am J Clin Pathol 1997; 108: Wills ML et al. Incidence of high grade prostatic intraepithelial neoplasia in sextant needle biopsy specimens. Urology 1997; 49: Bostwick DG. Prospective origins of prostate carcinoma. Prostatic intraepithelial neoplasia and atypical adenomatous hyperplasia. Cancer 1996; 78: Park S, Shinohara K, Grossfeld GD, Carroll PR. Prostate cancer detection in men with prior high grade prostatic intraepithelial neoplasia or atypical prostate biopsy. J Urol 2001; 165: O dowd GJ et al. Analysis of repeated biopsy results within 1 year after a noncancer diagnosis. Urology 2000; 55: Riffenburgh RH, Amling CL. Use of early PSA velocity to predict eventual abnormal PSA values in men at risk for prostate cancer. Prostate Cancer Prostatic Dis 2003; 6: Uzzo RG et al. The influence of prostate size on cancer detection. Urology 1995; 46: Karakiewicz PI et al. Outcome of sextant biopsy according to gland volume. Urology 1997; 49: Mc Neal JE, Redwine EA, Freiha FS, Stamey TA. Zonal distribution of prostatic adenocarcinoma: correlation with histological pattern and direction of spread. Am J Surg Pathol 1988; 12: Lindert KA. Bacteremia and bacteriuria after transrectal ultrasound guided prostate biopsy. JUrol2000; 164:

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