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Original Article

Does extended prostate needle biopsy improve the concordance of Gleason scores between biopsy and prostatectomy in the Taiwanese population?

Yang, Ching-Weia; Lin, Tzu-Pinga,b,*; Huang, Yi-Hsiua,b; Chung, Hsiao-Jena,b; Kuo, Junne-Yiha,b; Huang, William J.S.a,b; Wu, Howard H.H.a,b; Chang, Yen-Hwaa,b; Lin, Alex T.L.a,b; Chen, Kuang-Kuoa,b

Author Information
Journal of the Chinese Medical Association: March 2012 - Volume 75 - Issue 3 - p 97-101
doi: 10.1016/j.jcma.2012.02.001

    Abstract

    1. Introduction

    The Gleason score is an important parameter in the treatment of prostate cancer. The principle of the grading system for prostate cancer, which was first introduced by Gleason and Mellinger, has gained wide acceptance as the standard grading system in clinical urological practice.1 On the practical level, the Gleason score helps practitioners determine the likelihood of cancer recurrence in patients after radical prostatectomy and is also correlated with the prognosis of prostate cancer.2,3 However, several investigators have reported discordance between the Gleason scores of prostate biopsy and the radical prostatectomy specimens.4–8

    The sextant biopsy technique is the standard method for routine prostate biopsy for diagnosing prostate cancer. However, data on patient populations in Western countries has shown that the diagnostic accuracy of prostate cancer improves when ≥10 cores are taken using extended biopsies.9,10 Of primary interest here is whether an extended biopsy improves the grading accuracy of prostatectomy in the Taiwanese population as well.

    In 2004, urologists in Taipei Veteran General Hospital started performing extended needle biopsies (> 10 cores) for the diagnosis of prostate cancer by obtaining samples from the prostate as well as additional biopsies of any areas that appeared suspicious on digital rectal or ultrasound examinations. We investigated the exact concordance of the Gleason scores of the preoperative needle biopsies and prostatectomy specimens as the number of cores obtained by needle biopsy increased. We also analyzed potential upgrading in prospective candidates for active surveillance. Active surveillance is safe for low-risk prostate cancer and is an alternative to prostatectomy for all newly diagnosed men.11

    2. Methods

    From March 2000 to September 2009, 281 patients who underwent radical prostatectomy procedures at our institution were identified and enrolled in this study. The present project was approved by the institutional review board. We divided the cohort into two groups according to the number of cores obtained by 18-gauge transrectal needle biopsy: the first group had an extended number of cores (≥ 10 cores, range: 10–13, median: 12, obtained from 2005–2009); the second group had a nonextended number of cores (< 10 cores, range: 6–9, median: 6, obtained from 2000–2004). Group 1 was comprised of 121 patients who were diagnosed with cancer by extended biopsy. Group 2 was comprised of the remaining 160 patients who underwent nonextended biopsy before undergoing radical prostatectomy. The concordance rate was established by comparing the Gleason score of the prostate biopsy with the prostatectomy pathology, which is considered the gold standard of assessment. We compared the concordance rates between the extended and nonextended groups. The patients who fit the criteria of active surveillance which was defined as PSA ≤ 10 ng/mL, Gleason score ≤6 by biopsy, and negative digital rectal examination were analyzed as a subgroup. The pathology results were reported by two well-trained uropathologists in our pathology department. Preoperative clinical variables were assessed in both groups, including patient age, serum PSA, number of biopsy cores, Gleason scores, and time until an operation for prostate cancer. The Student t test and the χ2 test were used for comparisons of the clinical variables between the two groups.

    3. Results

    The baseline characteristics of the patients are listed in Table 1, including age, PSA, pathological stage, Gleason score, and median number of cores obtained from each patient in each of the two groups. The characteristics are similar between both groups. Median patient ages were 67 and 69 years, the median prebiopsy PSA levels were 16.62 ng/mL (range: 0.5–227 ng/mL) and 14.75 ng/mL (range: 2–187 ng/mL) for the extended and nonextended biopsy groups, respectively. The Gleason score of the prostate biopsy was 5 or 6 in 177/281 cases (63%). One hundred and fifty-four of the 281 patients (55%) turned out to be pT2 after radical prostatectomy. The Gleason score obtained from the biopsies compared to those obtained from the prostatectomies are plotted in Tables 2 and 3. The average number of biopsies was 1.142. The concordance rates between the biopsy and prostatectomy specimens are 50.2% (111/221), 43.8% (7/16), 100% (4/4), and 50% (2/4) in the divided groups who received one, two, three, or more than three prostate biopsies, respectively (Fisher's exact test, p = 0.239).

    Table 1
    Table 1:
    Clinical and pathological characteristics of men undergoing prostatectomy.
    Table 2
    Table 2:
    Gleason score concordance for nonextended biopsies (<10 cores).
    Table 3
    Table 3:
    Gleason score concordance in extended biopsies (≥10 cores).

    The concordance of the Gleason score sum between the needle biopsies and the radical prostatectomies was 70/121 cases (57.9%) and 73/160 cases (45.6%) for extended and nonextended biopsies, respectively (p = 0.042). Upgrading occurred in 43/121 cases (35.5%) in the extended biopsy group and 63/160 cases (39.4%) in the nonextended biopsy group (p = 0.511). Downgrading occurred in 8/121 cases (6.6%) in the extended group and 24/160 cases (15.0%) in the nonextended biopsy group (p = 0.028). Regarding the primary Gleason pattern, biopsy and prostatectomy concordance was 98/121 cases (81.0%) and 112/160 cases (70%) for extended and nonextended biopsies, respectively (p = 0.032), as seen in Table 4. The Gleason scores of 47/281 patients (16.7%) who fit the criteria for active surveillance (preoperative Gleason score ≤6 and PSA ≤ 10 ng/mL) were upgraded to >7 after radical prostatectomy. Among the potentially active surveillance group, upgrading occurred in 17/121 cases (14.0%) of extended biopsy and does not demonstrate a statistically significant improvement over nonextended biopsy in 30/160 cases (18.7%) (p = 0.296).

    Table 4
    Table 4:
    The concordance of Gleason score in extended and non-extended between prostate needle biopsies and prostatectomy specimens.

    4. Discussion

    The treatment options for localized prostate cancer should be based on accurate information, including both clinical parameters (age, comorbidity, PSA level, and results of the digital rectal examination) and pathological parameters (Gleason score). Of these parameters, the Gleason score for prostate cancer is one of the most important predictors of cancer recurrence and prognosis. The Partin Coefficient Tables, which are based on the PSA level, Gleason score, and clinical stage, are an important tool for guiding decisions about effective treatment options for prostate cancer. Individually processed needle biopsies lead to a better and more accurate diagnoses of prostate cancer, according to an earlier study.12 The best concordance was achieved when >12 core biopsies were obtained.

    In Western countries, San Francisco et al13 compared 126 patients with ≥10 cores with 311 patients with ≤9 cores. The concordance rate was 100/126 cases (79%) and 233/340 cases (68%) for extended and nonextended biopsies, respectively (p = 0.008). P. Emiliozzi et al14 demonstrated that the concordance of Gleason scores between prostate biopsy and radical prostatectomy was 32/46 cases (70%) and 44/89 cases (49%) for 12-core and 6-core transrectal biopsies, respectively (p = 0.0127).

    Regarding Asian populations, Miyake et al15 reported a concordance rate of 57/107 cases (53.3%) and 82/118 cases (69.5%) in non-extended (median: 8 cores) and extended groups (median: 12 cores) in Japan. Multivariate analysis identified the number of biopsy cores and the percent of positive biopsy cores as independent predictors of accurate Gleason grading. Our study suggests that the use of extended biopsies is beneficial, whereas extended biopsies produce a higher concordance rate with Gleason scores (70/121 cases, 57.9%) over nonextended biopsies (73/160 cases 45.6%, p = 0.042). Our concordance rate is a little lower than, but comparable to, the Japanese study. The reason may be that we had a lower mean number of cores that were obtained compared with the Japanese study.

    In Korea, 995 patients who underwent 12-core biopsies and 468 patients who underwent sextant biopsies of the prostate demonstrated that the 12-core biopsy detects cancer more accurately than 6-core biopsy in patients with a PSA density in the range 0.1–0.2.16 However, one prospective randomized study17 showed no significant difference in the prostate cancer detection rate between the 6-core biopsy group (14.4%, 17/118) and the 12-core biopsy group (17.2%, 21/122), based on different PSA levels, ages, and prostate volumes (p = 0.60). The number of patients may be the cause of this lack of significance. This study also didn't show the concordance rate according to pathological results after prostatectomy. Because of the lack of consistency between study results in the literature, we were motivated to study this issue in a Taiwanese population.

    The existing literature suggests that the upgrading of the Gleason score of needle biopsy specimens with prostatectomy is more common than downgrading.13,14,18–21 Our study supports this viewpoint, with an upgrading rate of 37.7% and a corresponding downgrading rate 11.4%. Gleason described the most probable cause of this in 1992: “Some upgrading is simply sampling error in small needle biopsies. Some pathologists actually seem reluctant to recognize small amounts of higher grade tumor if the total amount of the tumor on the biopsy is very small.” We agree with this explanation and believe that, as demonstrated in our study, a higher number of cores yields a higher accuracy rate. Extended transrectal biopsy also had a lower rate of downgrading (p = 0.028) the Gleason score than nonextended biopsies. When extended biopsy was performed, it seemed to decrease the frequency of upgrading in this study, but this did not reach the level of statistical significance (p = 0.511). The limited number of cases may be one reason; the other reason may be due to a single pathologist's review because different pathologists may base their interpretations on the small amount of the specimen and may hesitate to identify a higher grade of prostate cancer.

    However, Chen et al22 reported that transurethral resection of the prostate (TURP) is not superior to transrectal ultrasound-guided biopsy (12 cores) for detecting prostate cancer, even when large prostate specimens are available. Prostate cancer is more prevalent in the peripheral zone than the transitional zone, and lower grade tumors were more prevalent in the TURP group (11.1%).

    Previous studies investigating prostate volume demonstrated a significantly higher positive biopsy yield in prostates with a volume <50 cc compared with those 50 cc.23,24 Recently, Dong et al25 discussed the predictive factors associated with pathological upgrading after prostatectomy, noting that a prostate weight of ≤60 g (p = 0.004) is more frequently associated with upgrading. The conclusions reached by these authors suggest that the number of prostate biopsies should be guided by the prostate volume. In our series, we divided prostate volume into two groups: one group had larger volume more than 50cc and the other group had smaller volume less than 50cc. In the larger volume group, the concordance rate between biopsy and prostatectomy specimens was 67% and 56%, respectively, (χ2 test, p = 0.361) in the extended and nonextended group. In the smaller volume group, the concordance rates were 52% and 42% (p = 0.174), respectively. There was no significant change in the accuracy rate when we divided the prostate volume by 40 mL or 30 mL (p = 0.187 and p = 0.553, respectively). We didn't prove that extended core biopsy increases the Gleason score accuracy rate when adjusted for prostate volume. Considering the consistent superiority of the extended biopsy, the lack of significance is most likely due to the relatively small sample size.

    In a prospective study in Toronto,11,26 active surveillance was considered as an established treatment alternative, especially in clinical stage T1c or T2a prostate cancer with a Gleason score ≤6 and a serum PSA ≤ 10 ng/mL. In our series, Gleason scores of 5 or 6 account for the majority of 70/121 (60.3%) and 104/160 (65.0%) cases in the extended and non-extended biopsies, respectively (p = 0.785). We found that 47/281 patients (16.7%) who fit the active surveillance criteria were preoperatively upgraded to a Gleason score sum >7 after examination of their radical prostatectomy specimens. Köksal et al27 also reported a discrepancy in Gleason scores between prostate biopsy and radical prostatectomy specimens. Twenty-seven of 110 cases (25%) with a biopsy Gleason score <7 had their cancers upgraded to 7. Of the patients with both a Gleason score <7 on needle biopsy and a Gleason score of 7 on the prostatectomy specimen, only 3 (11%) had tumor activity that was confined to the prostate. This discrepancy affects the treatment policy, especially with regard to the active surveillance criteria. In our study, we found that the upgrading rate (Gleason score of 6 upgraded to 7) in the potential active surveillance group was 17/121 (14.0%) and 30/160 (18.7%) in the extended and nonextended biopsies (p = 0.296). The upgrading rate did not reach statistical significance probably due to the limited sample size of our study. Klotz11 emphasized the better policy of repeating the prostate biopsy after 1 year, or when an elevated PSA level is recorded on a regular follow-up examination, due to the fact that high-grade prostate cancer could have been missed on the original biopsy. Our findings are consistent with the bulk of the evidence that supports repeated biopsies and extended biopsies when active surveillance is an option.

    The central limitation of our study is the nature of this retrospective review. One factor that possibly impacts our study is the duration of the study itself, since the extended needle biopsies were performed between 2000–2004, as compared with the nonextended biopsies which were performed between 2004–2009. We also noted the lack of a single pathologist review (one experienced urological pathologist responded to 79% of the pathological reports), the variation in the interval until the operation was received, and different prostate volumes between the two groups.

    Are increased transrectal needle biopsy cores needed in the active surveillance of low-risk prostate cancer? Our study results suggests that an increase in the number of core biopsies will increase the prostate cancer concordance rate, though it may require a larger cohort in order to narrow the answer of this question to a particular number; thus, further investigations are warranted.

    Acknowledgments

    Hui-Chen Lee, Division of Experimental Surgery & Biostatistics Task Force. This study is sponsored by a grant from the Veteran General Hospital, Taiwan (grant no. V99B1-022).

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    Keywords:

    Gleason score; grade migration; needle biopsy; prostatectomy; prostatic neoplasm

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