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Keywords:

  • prostate carcinoma;
  • prostate biopsy;
  • prostate specific antigen;
  • transperineal;
  • transrectal

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES

BACKGROUND

The authors evaluated a new age-adjusted and prostate volume-adjusted biopsy method for the detection of prostate carcinoma through the transperineal and the transrectal approaches in men with PSA levels of 4.1–10.0 ng/mL.

METHODS

The value of the adjusted biopsy method was calculated by using the following four factors: 1) life expectancy in Japanese men in 1998, 2) prostate volume estimated by transrectal ultrasonography, 3) tumor doubling time (4 years), and 4) tumor volume that influenced death (20 cc). The number of biopsy sites was set at 8–20. Between August, 1999 and December, 2001, 100 men age ≤ 79 years with prostate specific antigen (PSA) levels of 4.1–10.0 ng/mL underwent age-adjusted and volume-adjusted, systematic prostate biopsy.

RESULTS

The detection rate for the adjusted biopsy method was 46% (46 of 100 men). The clinical stage of prostate carcinoma was Stage II in 85% of patients and Stage III in 15% of patients. If routine six-sextant biopsy had been performed in all of the men who underwent adjusted systematic biopsy, then 15 of 46 patients (33%) with prostate carcinoma would have been missed. The detection rates of prostate carcinoma in men who underwent adjusted biopsies were relatively high, especially in men with PSA levels of 6.1–10.0 ng/mL, men age ≤ 64 years, men with prostate volumes ≥ 50 cc, and men with PSA density (PSAD) levels ≤ 0.15 ng/mL/cc compared with the detection rates from six-sextant and directed biopsies. The high detection rates were observed from biopsy sites at the posterior aspect of the lateral lobe through both the transperineal approach and the transrectal approach and at the anterior aspect of the transition zone through the transperineal approach.

CONCLUSIONS

The age-adjusted and prostate volume-adjusted prostate biopsy method was more useful for detecting clinically significant disease compared with the traditional six-sextant biopsy method. This adjusted biopsy method was especially useful in patients age ≤ 64 years, patients with large prostate volumes (≥ 50 cc), and patients with PSAD levels ≤ 0.15 ng/mL/cc. The authors recommend that patients undergo an additional transition zone biopsy at the anterior aspect through the transperineal approach. Cancer 2002;95:2112–9. © 2002 American Cancer Society.

DOI 10.1002/cncr.10941

Several studies have demonstrated the limited sensitivity of a single-sextant biopsy session,1–6 especially in patients with large prostate volumes.7–9 Eskew et al. reported that the disease detection rate using the five-region prostate biopsy technique was significantly better compared with conventional sextant biopsies.10 The usefulness of multiple-core prostate biopsies has been confirmed, although the optimal number of biopsies required remains controversial. It is suggested that a clinically significant tumor volume at the time of diagnosis depends on the patient's age; thus, the adequate number of biopsy specimens may be different according to both individual prostate volume and age. Vashi et al. investigated a model for the number of cores per prostate biopsy based on patient age and prostate gland volume,11 although the usefulness of these biopsy methods was not evaluated. Thus, few studies have compared transperineal biopsy and transrectal biopsy methods.12 In the current study, we evaluated a new age-adjusted and prostate volume-adjusted biopsy method combined with transperineal and transrectal routes, and we propose efficient biopsy sites and approaches.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES

Calculating Parameters for the Age-Adjusted and Volume-Adjusted, Systematic Biopsy Method

The average life expectancy was investigated based on a life table for the Japanese population in 1998. The tumor doubling time was set at 4 years based on the findings of Schmid et al.,13 and the tumor volume that influenced death was set at 20 cc based on the study of Dugan et al.14 The tumor volume at which a diagnosis is necessary for each age was calculated using the following formula: Z = 2(Y/DT) × X, where Z is the tumor volume after the year Y, DT is the tumor doubling time in years, and X is the tumor volume at the time of diagnosis. With the tumor doubling time set at 4 years, the tumor volume that influenced death set at 20 cc, and Y as the calculated life expectancy for Japanese, X is the tumor volume and is calculated using the following formula: X = 20 cm3/2(Y/4).

Using that calculation, the tumor volumes at which diagnosis is necessary at each age are shown in Table 1. Simultaneously, the prostate volume was calculated from the findings on transrectal ultrasonography (TRUS), and the necessary number of biopsies for the diagnosis relative to the tumor volume was set based on the study of Vashi et al.11 Finally, the necessary number of biopsies for each age range and prostate volume was determined (Table 2). In this clinical study, the number of prostate biopsies was set to at least eight sites.

Table 1. Tumor Volume for Each Age Group
Age (yrs)505560657075
Tumor volume (cc)0.120.260.531.11.93.3
Table 2. Number of Cores per Biopsy to Ensure 90% Certainty of Detecting Disease as a Function of Prostate Gland Size and Patient Age
Prostate volume (cc)Age (yrs)
50–5455–5960–6465–6970–7475–79
< 19201210644
20–291814884
30–39201812106
40–492014106
50–5916128
60–80201810

Clinical Experience

Between August 1999 and December 2001, 100 men ages 50–79 years (mean ± standard deviation, 68.2 ± 6.2 years) with prostate specific antigen (PSA) levels of 4.1–10.0 ng/mL underwent age-adjusted and volume adjusted-biopsy using TRUS through both the transperineal approach and the transrectal approach. The number of age-adjusted and volume-adjusted biopsies was set at 8–20 (Fig. 1). Additional TRUS-guided biopsies were performed at the hypoechoic region, and additional digital rectal examination (DRE)-guided biopsies were performed at the nodular region. The prostate volumes were calculated by using the three-axis method (length × weight × height × 0.52). PSA density (PSAD) was calculated by dividing the serum PSA level by the prostate volume. All procedures were performed using the Bruel Kjaer model with a biplaner 5.0–7.5 MHz endorectal probe, and biopsies were obtained using an 18-gauge core biopsy needle with a spring-loaded biopsy (Bard Urological, Covington, GA). PSA levels were measured in all men using an E-test Tosoh II PA kit (Tosoh, Tokyo, Japan). The 1997 International Union Against Cancer (UICC) TNM classification of prostate carcinoma was used. The Gleason scores for all patients with prostate carcinoma were reviewed by one urologic pathologist for this study. Tumors were considered clinically significant if patients had a Gleason score > 6, if > 1 biopsy core was involved, or if > 3 mm were involved on 1 core.15

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Figure 1. The region of prostate biopsy is illustrated using the age-adjusted and prostate volume-adjusted systematic biopsy method in transverse and longitudinal views. The biopsy cores from the posterior aspects of Regions 1–3 in the peripheral zone were obtained with both transperineal and transrectal approaches. The biopsy cores from the anterior aspect of Region 1 in the peripheral zone and transition zone were obtained using the transperineal approach. TZ: transition zone; PZ: peripheral zone; SV: seminal vesicle; U: urethra; solid circles: six-sextant biopsy site with the transperineal approach, open circles: additional biopsy site through the transperineal approach; solid vertical arrows: six-sextant biopsy site through the transrectal approach; open vertical arrows: additional biopsy site through the transrectal approach; solid horizontal arrows: biopsy site in longitudinal view through the transperineal approach; open slanted arrow: biopsy site in longitudinal view through the transrectal approach.

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RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES

The clinicopathologic features of the patients with prostate carcinoma are shown in Table 3. Of 100 men who underwent age-adjusted and volume-adjusted biopsies, 46 men (46%) with prostate carcinoma were detected. Their ages ranged between 52 years and 79 years (mean ± standard deviation, 69.5 ± 5.8 years). The Gleason score ranged from 5 to 9, with a median Gleason score of 7. A total of 28 patients (60.9%) had positive biopsy cores with a Gleason score of 4 or 5. The number of positive biopsy cores ranged from 1 to 8 cores, with a mean of 2.3 cores.

Table 3. Clinicopathologic Features of Patients with Prostate Carcinoma who Underwent Age- and Prostate-Volume-adjusted Prostate Biopsy with Prostate Specific Antigen Levels of 4.1–10 ng/mL
FeatureNo.%
Patients with prostate carcinoma46100
No. of positive biopsy cores  
 11941.3
 2–31941.3
 4–548.7
 6–736.5
 8+12.2
Clinical stage  
 T1c/T2N0M03984.8
 T3N0M0715.2
 N1 or M100.0
Gleason score  
 5–61839.1
 71941.3
 8–9919.6
Gleason Grade 4 or 5  
 Primary919.6
 Secondary only1941.3

The proportion of patients with clinical Stage II disease was 84.8% of patients who underwent age-adjusted and volume-adjusted biopsy. A total of 44 patients (95.7%) with prostate carcinoma was clinically significant.

The detection rates of prostate carcinoma with the age-adjusted and prostate volume-adjusted biopsy method and with the six-sextant and directed biopsy methods according to various clinical findings are shown in Table 4. The detection rates for each category in men who underwent age-adjusted and volume-adjusted biopsy were higher for the most part compared with the detection rates for the six-sextant biopsy method alone. The detection rates of prostate carcinoma for men ages 50–64 years who underwent age-adjusted and volume-adjusted biopsy with were approximately 3-fold higher compared with the detection rates for men who underwent six-sextant biopsy. The detection rates according to prostate volume in men who underwent six-sextant biopsy decreased relative to prostate volume; however, the rate was relatively high at 43.5% in men who had prostate volumes ≥ 50cc who underwent age-adjusted and volume-adjusted biopsy. The detection rate with six-sextant biopsy was low at 17.5% in men with PSAD levels ≤ 0.15 ng/mL/cc; however, the rate increased to 35% for men who underwent age-adjusted and volume-adjusted prostate biopsy. For men who had no abnormal findings on DRE and TRUS, the detection rates for men who underwent age-adjusted and volume-adjusted biopsy were 1.6-fold and 2.0-fold higher, respectively, compared with men who underwent six-sextant biopsy. The detection rates according to the number of biopsy cores observed were approximately 2-fold higher in men who had ≥ 14 prostate biopsy cores compared with the detection rates in men who underwent six-sextant biopsy. The high detection rate for men who had 8–10 biopsy cores was observed mainly in those who underwent an additional biopsy of the anterior aspect of the transition zone using the transperineal approach.

Table 4. Detection Rate According to Prostate Specific Antigen Level, Age Distribution, and Findings on Digital Rectal Examination and Transrectal Ultrasonography
Clinical findingsNo.Detection rate (%)No. of patients with prostate Ca detected from SSB and/or DB siteDetection rate (%)
ScreeneesDiagnoses
  1. Ca: carcinoma; SSB: six-sextant biopsy; DB: directed biopsy; PSA: prostate specific antigen; DRE: digital rectal examination; TRUS: transrectal ultrasonography.

PSA (ng/mL)     
 4.1–6.0461737.01430.4
 6.1–10.0542953.71731.5
Age range (yrs)     
 50–5910330.0110.0
 60–6418527.8211.1
 65–69251144.01040.0
 70–74301963.31343.3
 75–7917847.1529.4
Prostate volume (cc)     
 − 24161381.31168.8
 25–49612337.71626.2
 50+231043.5417.4
PSA density (ng/mL/cc)     
 − 0.15401435.0717.5
 0.16–0.25371437.8924.3
 0.26 +231878.31565.2
DRE     
 Not suspicious for Ca733243.82027.4
 Suspicious for Ca271451.91140.7
TRUS     
 Not suspicious for Ca552240.01120.0
 Suspicious for Ca452453.32044.4
No. of biopsy cores observed     
 8–10412561.01639.0
 11–13211257.11152.4
 14–1717423.5317.6
 18–2121523.814.8

The positive biopsy sites in men who underwent age-adjusted and volume-adjusted biopsy are shown in Table 5. The positive biopsy rates in the peripheral zone and the transitional zone were 7.2% and 8.3%, respectively. High detection rates were observed from biopsy sites in the posterior aspect in Region 1 through the transperineal approach, transrectal biopsy at Region 1, and the anterior aspect of the transition zone through the transperineal approach. The detection rate was low at 1.4% (1 of 72 men), 2.2% (1 of 46 men), and 3.8% (3 of 80 men) at the biopsy sites from transrectal biopsies of Region 2 and Region 3 and from the posterior aspect of the transition zone through the transperineal approach, respectively. The detection rates of biopsy sites from the anterior aspect of Region 1, Region 2 and Region 3 through the transperineal approach were relatively high at 5.5%, 7.1%, and 6.6%, respectively.

Table 5. Positive Biopsy Site in Patients with Prostate Carcinoma
Biopsy siteNo. of biopsy sitesPositive for carcinoma
No. of biopsies%
  1. PZ: peripheral zone; TZ: transition zone; TRUS: transrectal ultrasonography; DRE: digital rectal examination.

PZ993717.2
TZ290248.3
Total1283957.4
Systematic biopsy   
 Transperineal biopsy of PZ   
  Anterior aspect of region 1200115.5
  Posterior aspect of region 12012210.9
  Region 2140107.1
  Region 310676.6
 Transrectal biopsy of PZ   
  Region 12012110.4
  Region 27211.4
  Region 34612.2
 Transperineal biopsy of TZ   
  Anterior aspect200199.5
  Posterior aspect8033.8
Directed biopsy (including systematic biopsy site)   
 Hypoechoic region on TRUS491530.6
 Nodular region on DRE10550.0
No. of patients stratified by positive biopsy site   
 Including routine six sextant biopsy site2963.0
 Including directed biopsy site1123.9
 Except for routine six-sextant and directed biopsy site alone   
  Both PZ and TZ36.5
  PZ only36.5
  TZ only919.6

Among 46 patients with prostate carcinoma, 15 men (32.6%) had disease that was detected as prostate carcinoma at the biopsy site except for routine six-sextant and DRE-guided and/ or TRUS-guided, site-directed biopsies. Of these 15 patients with prostate carcinoma, 9 men (60%) had disease that was detected at the transition zone through the transperineal approach alone. If six-sextant biopsy and DRE-guided and/ or TRUS-guided, site-directed biopsy had been performed in all of the men who underwent age-adjusted and volume-adjusted biopsy, then the detection rate would have decreased to 31% (31 of 100 men), and 15 of 46 men (35%) with prostate carcinoma would had been missed. Among these 15 men with prostate carcinoma, only 1 man (6.3%) was expected to have a clinically insignificant tumor with a Gleason score of 6 and a greatest tumor dimension of 2.6 mm.

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES

The age-adjusted incidence of prostate carcinoma in Japanese males is very low, approximately 10 in 100,000 population, compared with 147.3 in 100,000 population for white American males and 222.9 in 100,000 population for black American males;16 however, the prostate carcinoma detection rate of 2.3% in Japanese males17 was not different from the incidence of 1.5–4.1% in American males18–21 when we undertook PSA-based, systematic screening for the first time. Subsequently, several studies reported that the detection rate was between 18.9% and 33.0% in men who underwent six-sextant biopsy with PSA levels of 4.1–10 ng/mL,18, 22–25 and the detection rate for Japanese males was not different22 from that of American males with PSA levels in the same range.

It is expected that some clinically significant tumors would have been missed in patients undergoing six-sextant biopsy. A few studies demonstrated the detection rates of serial prostate biopsy in men with negative initial biopsy findings.1, 2 Keetch et al. demonstrated that the detection rates of prostate carcinoma in men with suspicious findings on serum PSA values, DRE, or TRUS and negative previous biopsy findings were 34%, 19%, 8%, and 7% on the first, second, third, and fourth set of prostate biopsies, respectively.1 Borboroglu et al.2 carried out repeat biopsies in 57 men with negative biopsy findings for prostate carcinoma in the first biopsy, and the detection rate of repeat biopsy for prostate carcinoma was 30%. Those authors proposed that a repeat biopsy should be undergone by men who have clinical findings that are suspicious for prostate carcinoma.

Several studies have demonstrated the usefulness of multiple-core biopsy for the detection of prostate carcinoma. Eskew et al. reported that the detection rates of systematic five-region prostate biopsy for prostate carcinoma increased to 55% compared with the detection rates of systematic six-sextant biopsies.7 A comparison between the detection rates of six-sextant biopsy and multiple-core biopsy are not possible with simplicity, although the detection rates of multiple-core biopsy were high at 30.0–45.0%.7, 23, 26 Chang et al. reported that the detection rate for prostate carcinoma was 43.5% in men who underwent multiple-core biopsies with PSA levels of 4–10 ng/mL.27 The high prostate carcinoma rate (46%) was also demonstrated among an Asian population with PSA levels of 4–10 ng/mL in the present study.

An important point in the current study is accepting the concepts proposed by Vashi et al.11 that the cut-off value for the clinically important tumor volume should be decided according to the age of the patient and that the number of biopsies should be determined according to the factors of patient age and prostate volume. McNeal et al. demonstrated that 17 of 33 patients (52%) with prostate carcinoma who had tumor volumes > 0.46 mL showed capsular penetration; however, only 4 of 56 patients (7%) with prostate carcinoma who had tumor volumes < 0.46 mL had capsular penetration.28 The tumor volume of 0.46 mL is considered one of the clinically important cut-off values. In the current study, the clinically important tumor volume was calculated by using data on life expectancy, tumor doubling time, and tumor volume that influenced death. The tumor doubling time is related strongly to tumor behavior, and there were various tumor doubling times in our clinical setting; however, the 4-year tumor doubling time indicated in this study is considered valuable as a mean tumor behavior. For example, in the current study, the calculated, clinically significant tumor volume for patients age 60 years using our formula, as discussed above, was 0.53 cc. That was almost the same as the clinically important cut-off tumor volume demonstrated by McNeal et al. Therefore, the cut-off value for the tumor volume for patients age 60 years is considered valid. The calculated, clinically significant tumor volume of patients age 50 years was small at 0.12 cc; however, the life expectancy for Japanese men age 50 years is almost 30 years, so that the tumor volume of 0.12 cc also was valid as the clinically important tumor volume.

Some previous studies have demonstrated that positive biopsy rates are affected by prostate volume and patient age. Uzzo et al. demonstrated that the positive biopsy rate was significantly higher at 38% in men who had prostate volumes < 50 cc compared with men who had prostate volumes ≥ 50 cc (23%) based on a review of 1021 six-sextant biopsies.10 In the current study, the positive biopsy rate decreased in men who underwent age-adjusted and prostate volume-adjusted biopsies accompanied by an increasing prostate volume, but it was small compared with the reduced detection rate of prostate carcinoma by six-sextant biopsy and directed biopsy, and the observed detection rates were high (43.5%) in men with prostate volumes ≥ 50 cc.

Orozco et al. demonstrated that the positive biopsy rate consistently increased with age at similar PSA levels in patients with normal DRE and PSA levels of 4–10 ng/mL.29 Those authors hypothesized that serum PSA may cause a benign rise by chronic inflammation in younger men, although prostate volume became greater in older men, so that the PSAD must be high in younger men who have equal PSA values. In addition, we also can hypothesize that the lower detection rates in younger men were the result of the lower disease volume in younger men when equal numbers of biopsies were obtained from both younger and older men with equal PSA values. In the current study, the positive biopsy rate was relatively high at 28.6% (8 of 28 men) in men age ≤ 64 years who underwent age-adjusted and prostate volume-adjusted biopsy and who had extraordinarily high numbers of biopsies; therefore, our theoretical idea described above also may be correct, and this adjusted biopsy method appears to be effective for the detection of important malignancies among men in the younger age group.

Several studies have demonstrated the diagnostic significance of the transition zone biopsy through the transrectal approach. Fowler et al. performed two transition zone biopsies, and only 7 of 565 men (1.2%) with prostate carcinoma had disease that was detected from the transition zone alone: Of those 7 patients with prostate carcinoma, 6 patients had a Gleason score of 2–6, and the authors asserted that there was no necessity for the routine transition zone biopsy.30 Other studies have demonstrated that the positive biopsy rates of repeat biopsy at two sites of the transition zone were 0% and 4.3% in men who had negative biopsy results at the peripheral zone.31–33 However, Chang et al. demonstrated that 13% of men with prostate carcinoma that was detected only from the transition zone underwent systematic sextant transition zone biopsies with prostate volumes ≥ 50 cc, and those authors asserted that such men should undergo a routine transition zone biopsy.34

In the current study, the positive biopsy rates per biopsy core were 7.2% (71 of 993 biopsy cores) and 8.3% (24 of 290 biopsy cores) in the peripheral zone and the transition zone, respectively. In addition, the detection rates per biopsy core were not significantly different between both biopsy sites. Of the 46 men who were diagnosed with prostate carcinoma, 9 men (19.6%) had disease that was detected only from the transition zone biopsy; and 7 of those 9 men (78%) had disease that was detected from the anterior aspect of the transition zone. There was little information with regard to the usefulness of transition zone biopsy through the transperineal approach. We have demonstrated high detection rates with transition zone biopsy through the transperineal approach. Therefore, we recommended that the anterior aspect of the transition zone should be added to routine prostate biopsy sites.

We performed extraordinarily high numbers of biopsies for men age ≈ 50 years or with large prostate volumes in this study; However, it appeared to be important to obtain an extraordinary high detection rate. We have to avoid overtreatment for any patients who had disease detected in such a preliminary study. In addition, we have proposed various treatment options (i.e., watchful waiting, radiation therapy, radical prostatectomy with or without prior endocrine therapy, and endocrine monotherapy) and have obtained informed consent for each patient relative to their tumor volume on biopsy cores, Gleason score, age, and performance status in this study.

We do expect that the age-adjusted and prostate volume-adjusted biopsy method described in this report will become the routine procedure rather than six-sextant biopsy. However, this method may become important when new serum markers can be used reliably in a clinical setting and can be adapted for use in prostate biopsy procedures in the future.

CONCLUSIONS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES

Of the 100 patients who underwent age-adjusted and volume-adjusted biopsy, prostate carcinoma was detected in 46 patients (46%). This biopsy method was more useful for diagnosing clinically significant disease compared with the traditional six-sextant biopsy method. If we had performed routine six-sextant biopsy for all of the patients who underwent age-adjusted and volume-adjusted systematic biopsy, then 33% of the patients with prostate carcinoma would have been missed. We should use this biopsy method, especially in men age ≤ 64 years, men with a large prostate volume (≥ 50 cc), or with PSAD levels ≤ 0.15 ng/mL/cc. In the current study, 20% of patients with prostate carcinoma had their disease detected only from the transition zone biopsy; thus, the additional transition zone biopsy should be performed at the anterior aspect through the transperineal approach.

REFERENCES

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. CONCLUSIONS
  7. REFERENCES
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