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Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 31  |  Issue : 4  |  Page : 170-176

Initial prostate biopsy of grade group one: A study of pathological upgrade and biochemical recurrence after robotic-assisted laparoscopic radical prostatectomy


Department of Urology, National Taiwan University Hospital, National Taiwan University College of Medicine, Taipei, Taiwan

Date of Submission29-Nov-2019
Date of Decision12-Feb-2020
Date of Acceptance23-Feb-2020
Date of Web Publication25-Jul-2020

Correspondence Address:
Yu-Chuan Lu
Department of Urology, National Taiwan University Hospital, College of Medicine, National Taiwan University, Number 7, Chung-Shan South Road, Taipei 100
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/UROS.UROS_91_19

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  Abstract 


Purpose: The aim of our study was to analyze the outcomes and predictive factors in patients with an initial biopsy grade group 1 (GG1) prostate cancer (PCa) at risk of GG upgrading. Materials and Methods: We performed a retrospective review of patients who had GG1 PCa at biopsy and were managed with robotic-assisted laparoscopic radical prostatectomy (RaLRP) from January 2012 to December 2018 and collected their clinical characteristics and pathological data. The primary outcomes were GG upgrading at RaLRP and biochemical recurrence-free survival (BCRFS) in these patients. The secondary outcome was to analyze the risk factors of pathological upgrades. Results: Among the 159 patients with initial prostate biopsy of GG1, 122 patients (76.7%) had GG upgrading based on the final pathology at RaLRP. Multivariable analysis showed that transrectal ultrasound (TRUS)-measured prostate volume <30 mL (odds ratio [OR] 4.727, P = 0.011), prostate-specific antigen density [PSAD] ≥0.2 ng/mL2 (OR 3.201, P = 0.019), magnetic resonance imaging (MRI)-measured prostate volume <30 mL (OR 3.892, P = 0.007), and PSAD ≥ 0.2 ng/mL2 (OR 2.65, P = 0.019) were independent predictive factors of GG upgrading. During 5 years of follow-up, patients who upgraded to GG3-5 had a significantly shorter time to biochemical recurrence than those who remained as GG1 (P = 0.001) or upgraded to GG2 (P = 0.008). Conclusion: The final pathology grading was underestimated in 76.7% of initial biopsy GG1 and may influence the BCRFS after RaLRP. Prostate volume <30 mL and PSAD ≥0.2 ng/mL2, measured by either MRI or TRUS, were significant predictive factors of biopsy GG1 upgrading.

Keywords: Gleason score, prostate biopsy, prostate cancer, radical prostatectomy, upgrade


How to cite this article:
Hung FC, Tseng CS, Chen CH, Chang HC, Huang CY, Lu YC. Initial prostate biopsy of grade group one: A study of pathological upgrade and biochemical recurrence after robotic-assisted laparoscopic radical prostatectomy. Urol Sci 2020;31:170-6

How to cite this URL:
Hung FC, Tseng CS, Chen CH, Chang HC, Huang CY, Lu YC. Initial prostate biopsy of grade group one: A study of pathological upgrade and biochemical recurrence after robotic-assisted laparoscopic radical prostatectomy. Urol Sci [serial online] 2020 [cited 2020 Nov 27];31:170-6. Available from: https://www.e-urol-sci.com/text.asp?2020/31/4/170/290862




  Introduction Top


Prostate cancer (PCa) is the second most frequently diagnosed malignant tumor among men in the world, accounting for 1.27 million new cases in 2018.[1] In the current era, the number of patients being identified with low-risk PCa according to the D'Amico criteria has increased mainly due to the widely used prostate-specific antigen (PSA) as a screening marker.[2] Different therapeutic modalities are usually selected based on PSA level, clinical or radiologic stage, and biopsy Gleason score (GS). As the definitive cancer diagnosis is made on the biopsy report, the GS from the prostate biopsy is an important factor for initial treatment planning.

The discrepancy between GS based on prostate biopsy and that determined by final pathologic specimen has been well described.[3] It is especially important in men undergoing treatment other than radical prostatectomy (RP), as the only tissue obtained is from the needle biopsy. It has been reported that around 30%–50% of patients with low-risk diseases experienced GS upgrading on analysis of specimens from RP,[4] while a higher pathological GS is associated with an increased risk of postoperative biochemical recurrence (BCR) and PCa-specific mortality.[5] Since patients with low-risk PCa may be monitored by active surveillance (AS), it is clinically crucial not to miss patients with aggressive tumors.

In 2016, the International Society of Urological Pathology (ISUP) Consensus Conference proposed a simplified grading system, Grade Groups (GGs) 1–5, in order to provide more accurate grade stratification.[6] While magnetic resonance imaging (MRI) is not recommended for local staging in low-risk patients,[7] it can be useful for treatment planning. In our practice, MRI is performed prior to RP and is covered by the National Health Insurance. To the best of our knowledge, few articles evaluate the use of MRI in predicting patients with GG1 upgrading.[8] According to 2019 NCCN guidelines, patients with GG3 PCa would be further stratified into unfavorable intermediate risk, in which active surveillance is not recommended. We intended to investigate the differences among those remaining as GG1, those upgraded to GG2, and those upgraded to GG3–5. Here, we aimed to identify significant clinical factors, including MRI findings, that predict upgrading of biopsy GG1 PCa by RP specimen, and the consequences on BCR outcome.


  Materials and Methods Top


Study population

In accordance with the Declaration of Helsinki, the Institutional Review Board of National Taiwan University Hospital approved the chart review for this study (protocol no. 201305059RINC). We identified 165 men who were originally diagnosed with GG1 PCa and underwent robotic-assisted laparoscopic RP (RaLRP) for PCa at our institution between January 2012 and December 2018. Follow-up data were obtained in March 2019. We collected patient data including the clinical characteristics, perioperative laboratory data, initial biopsy pathology reports, and final pathology after RaLRP. Patients with incomplete data or who received hormone therapy before RaLRP were excluded from the study.

Study design

Biopsy methods consisted of a 12-core systemic biopsy under the guidance of transrectal ultrasound (TRUS). In some cases, an additional TRUS-guided transperineal prostate biopsy was applied. When serial biopsy reports were identified in a single patient, the initial biopsy pathology was defined as the biopsy report before RaLRP. BCR was defined as PSA elevation over 0.2 ng/ml after RaLRP.[9] The primary outcomes were the pathology upgrading after RaLRP and their BCR-free survival (BCRFS) in each GG. The secondary outcome was to analyze the risk factors of BCR.

Pathology grading system

The patients were graded based on the suggestions of the 2014 ISUP meeting. Briefly, a 5-GG system based on GS was used: GG1 (GS ≤6), GG2 (GS 3 + 4 = 7), GG3 (GS 4 + 3 = 7), GG4 (GS = 8), and GG 5 (GS = 9–10).

Statistical methods

All statistical analyses were performed using SPSS statistical software, version 22.0 (IBM Corp, SPSS, Inc., Chicago, IL, USA). The Mann–Whitney U-test was used to compare medians between the patient groups. Contingency tables were constructed for comparisons using the Chi-square test. The Kaplan–Meier method was used for the construction of survival curves. The log-rank test was used to compare the duration of BCRFS between groups. Factors that showed significant differences in the univariate analysis and those of clinical importance were selected for the multivariable model. The cutoff values of PSAD and prostate volume were chosen according to previous studies.[10] All tests were two-tailed. P < 0.05 was considered statistically significant.


  Results Top


Clinical and pathological characteristics

Among 480 patients who underwent RaLRP, 165 patients had an initial biopsy GG1 PCa. Six patients had received androgen deprivation treatment prior to RaLRP and were excluded. Therefore, 159 patients were included in the final analysis. The characteristics of our study population are presented in [Table 1]. In the present study, the median age at diagnosis was 64-year-old, the median body mass index (BMI) was 24.8 kg/m 2, and the median of initial PSA level was 8.8 ng/mL. Among the 159 patients, 76.7% were in clinical T1 stage, and 50.5% were defined as low-risk prostate adenocarcinoma according to the D'Amico criteria. Based on the RaLRP specimen, GG was consistent with that of the initial biopsy in 37 cases (23.3%), and 122 cases (76.7%) had an upgraded GG.
Table 1: Clinical characteristics of the study population

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Association and predicting an upgrade from Grade Group 1

We stratified our study population into three groups: those remaining as GG1, those upgraded to GG2, and those upgraded to GG3–5. [Table 2] shows the association of preoperative clinical and pathologic variables with upgrades from biopsy GG1 after RaLRP. The upgraded patients were associated with higher BMI, smaller prostate volume, higher PSA density (PSAD) measured by either TRUS or MRI, and abnormal digital rectal examination (DRE) results. We did not identify any significant association between GG upgrade and the biopsy details including prior negative biopsy, bilateral positive biopsies, number of biopsy cores, positive cores, or maximum percentage of cancer per core.
Table 2: Clinical characteristics stratified by consistent grade group 1, upgrade to grade group 2, or upgrade to grade group 3-5

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In the univariate analyses, the predictors of GG1 upgrade were abnormal DRE (P = 0.049), TRUS-measured prostate volume <30 mL (P = 0.008), and PSAD ≥0.2 ng/mL 2 (P = 0.012). MRI-measured prostate volume <30 mL (P = 0.003) and PSAD ≥0.2 ng/mL 2 (P = 0.005) were also variables predicting an upgrading GG1 PCa [Table 3]. Parameters with P < 0.2 were selected for multivariate analysis. We used models 1 and 2 to demonstrate TRUS-measured prostate volume and PSAD and models 3 and 4 to indicate MRI-measured prostate volume and PSAD predicting an upgrading GG1 PCa. In the multivariable analyses, TRUS-measured prostate volume <30 mL (odds ratio [OR] 4.727, P = 0.011) and PSAD ≥0.2 ng/mL 2 (OR 3.201, P = 0.019), as well as MRI-measured prostate volume <30 mL (OR 3.892, P = 0.007) and PSAD ≥0.2 ng/mL 2 (OR 2.65, P = 0.019), remained independent predictive factors of GG1 upgrading [Table 4].
Table 3: Univariate analysis of the factors predicting pathology upgrading

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Table 4: Multivariate analysis of the factors predicting pathology upgrading

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Biochemical recurrence-free survival

The median follow-up time in our study was 24.8 months (IQR, 10.3–51.7 months). The 5-year BCRFS was 94.1% for those who maintained a GG1 diagnosis and was 79.8% for those who were upgraded to GG2–5. Patients who upgraded from GG1 to GG3–5 after RaLRP had a shorter time to BCR than those who remained as GG1 (P = 0.001) and those who upgraded to GG2 (P = 0.008) [Figure 1]. Smaller prostate volume measured by MRI and higher PSA level showed some tendencies of GG1 upgrading to GG3–5 and BCR [Figure 2].
Figure 1: Kaplan–Meier survival curves for biochemical recurrence-free survival in 159 prostate cancer cases according to grade group upgrade. (a) Grade group 1 consistent and grade group 1 upgraded to grade group 2–5. (b) Grade group 1 consistent, grade group 1 to grade group 2, and grade group 1 to grade group 3–5

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Figure 2: Scatter plots for (a) grade group 1 upgrade to grade group 3–5 by prostate-specific antigen level and magnetic resonance imaging-measured prostate volume, (b) biochemical recurrence by prostate-specific antigen level and magnetic resonance imaging-measured prostate volume

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  Discussion Top


In the recent decades, the implementation of serum PSA screening has resulted in better diagnosis of early-stage PCa, including for patients with GG1 disease. However, Gleason 4–5 components are associated with an increased risk of BCR, a need for adjuvant therapy, and increased PCa -specific mortality.[5] Identifying the patients at risk for GG upgrades is crucial, as clinicians may consider changing the treatment plan from Active Surveillance (AS) to active treatment.

Previous studies cited several reasons for the discrepancies between needle biopsy and RP GS: pathology error, borderline cases (the biopsy specimen may be categorized into two different grades), sampling error (a major component of the tumor in the RP is not present in the biopsy specimen), and reverse sampling error (a minor component of tumor in the RP is sampled in the biopsy specimen).[11],[12] In addition, intraobserver variability in biopsy GS assignment may be over 50%,[13] while interobserver variability can range from 22% to 37%.[14],[15] Investigations for sampling errors in larger prostate were discussed in previous studies: ≥8 systematic biopsies are recommended in prostates with a size of about 30 cc and 10–12-core biopsies were associated with more accurate grade prediction compared to 6-core biopsies and were recommended in larger prostates, while >12 cores were not significantly more conclusive. The protocol was compatible with this current study, with the median biopsy core number of 12.[16]

In the present cohort, the incidence of upgrading from GG1 was 76.7%. Four large European and American studies that each included more than 1000 patients reported GG1 upgrading rates ranging from 36.3% to 56.7%.[3],[4],[17],[18] A higher incidence of GG1 upgrade in our study may be attributable to the following reasons: (1) we did not perform routine confirmatory biopsy or systemic pathologic review of biopsy records, and interobserver variability could contribute to different results and (2) we used MRI imaging as one of the initial staging tools, and patients with adverse pathological features may be more likely to be detected, further leading to definitive surgery. According to a previously proposed nomogram, the well-known D'Amico risk stratification, clinical stage, serum PSA, and biopsy Gleason were all significant predictors for GS upgrade.[3] Epstein et al. reported that increased age, serum PSA, maximum percentage of cancer per core, and decreased RP weight all predict the upgrade from biopsy GS 5 to 6.[4] Audenet et al. found that age, abnormal DRE, PSAD, percentage of positive cores, and BMI were factors predicting an upgrade from GG1.[17] Seisen et al. suggested that the length of cancer per core, PSA, age, number of biopsy cores, and prostate weight were predictive variables for Gleason ≤6 upgrade.[18] In this present study, we found that prostate volume <30 mL and PSAD ≥0.2 ng/mL 2 were significant predictors for biopsy GG1 upgrade after RaLRP. Our results were compatible with several previous studies and suggested a smaller prostate size as an independent predictor of GS upgrading in low-risk PCa.[19],[20] A possible explanation is that smaller prostates may represent low in vivo androgenicity and can be associated with more aggressive, high-grade cancer.[21] In addition, Seisen et al. reported that a prostate weight >50 g evaluated by TRUS is a protective factor for an upgrade at RP from biopsy Gleason ≤6.[18] As larger prostates produce more PSA, large prostate sizes may consequently lead to increased detection of clinically insignificant cancers.[22] Although a linear correlation between pathologic weight and TRUS has been suggested,[21] some questions were raised about the accuracy of measuring prostate weight by TRUS due to interobserver variability. We avoided using postoperative pathologic weight for upgrade prediction. Instead, we incorporated preoperative prostate volume and showed that a smaller prostate predicted an upgrade of GG1 PCa measured by either TRUS (P = 0.011) or MRI (P = 0.007). The accuracy of the two different approaches was discussed. A previous study assessing prostate volume suggested that MRI was slightly more accurate than TRUS based on interclass correlation (0.83 vs. 0.74) when compared with surgical pathology. On average, MRI slightly overestimated prostate volume (mean 1.4 cc) and TRUS slightly underestimated prostate volume (mean − 3.4 cc).[23]

Previous studies reported increased PSAD as a predictor of upgrading, and it is associated with higher PSA levels produced by larger cancer volumes, in combination of the ascertainment bias associated with increased PSA detection of low-risk PCa from larger prostates.[24] PSAD has been suggested to be a stronger predictor for GG1 upgrade than PSA in a recent study.[25] We also found that PSAD ≥0.2 ng/mL 2 was an independent predictor of GG1 upgrading (P = 0.019).

It has been shown that patients with a GS upgrade on the final specimen exhibited significantly more aggressive pathological features compared with concordant tumors between biopsy and RP. Despite adjusting the preoperative variables, such as clinical stage, PSA, and the number and percentage of positive cores, upgrade to a higher GS remains a strong and independent predictor of post-RP BCR.[26] In a study of 6625 patients treated by RP, Müntener et al. found that patients with concordant GS (≤3 + 3, 3 + 4, and 4 + 3) at biopsy and RP had better 10-year BCRFS than those with GS upgrade at RP, and the authors suggested that biopsy GS could provide an additional prognostic value to the final specimen GS.[12] Compatible results were also noticed in our study, as GG1 patients' biopsy who were upgraded to GG3–5 at RP had a shorter time to BCR.

MRI has been described as a tool for the staging and detecting clinically significant PCa. In the PROMIS study, mpMRI was more sensitive than TRUS-P biopsy (93% vs. 48%) and less specific (41% vs. 96%) for clinically significant cancer, which was defined as GS ≥4 + 3 or a maximum cancer core length >6 mm.[27] Le et al. found that, in 122 men who underwent mpMRI before RP, the overall sensitivity for detecting GG3–5 tumors or tumors >1 cm was 72%; of the tumors missed on mpMRI, 75% were GG1, while only 4% were GG4–5.[28] Routine MRI study in patients who considered RP in daily practice may facilitate the identification of more aggressive diseases and consequently influence the treatment choices. Since all of our patients had MRI, this could be a possible reason for the higher biopsy GG1 upgrading rate in the present study. Some of our patients were diagnosed and received MRI imaging before the standardization of Prostate Imaging-Reporting and Data System (PI-RADS). As a result, we did not perform central imaging review and further analysis of the association between PI-RADS and pathological upgrading. Although the aforementioned comparisons were not evaluated in our work, a recent study suggested no difference in total numbers of lesions with MRI PI-RADS score 4 or 5 between GG1 nonupgrade and upgrade groups, while MRI PSAD was significantly associated with increased odds of upgrading on subsequent biopsy in an active surveillance cohort.[29] Furthermore, using MRI as an early confirmatory testing has been shown to improve risk classification and enhance the safe selection of patients for AS.[30]

There are several limitations in our study. It was a monocentric study with a relatively small sample size. No systemic pathologic review of biopsy records was performed, although interobserver variability was well-discussed before. Furthermore, the retrospective design inevitably leads to exclusion of some patients due to the lack of complete data for all variables. The selection of patients who underwent RaLRP might not be representative of the overall population. The survival analysis estimated with a median follow-up duration of 24.8 months should be considered as an immature assessment. Despite these limitations, this is the first study incorporating MRI-measured prostate volume for GG1 upgrading prediction, and our findings support the application of this additional indicator for low-risk PCa patients' stratification and treatment planning.


  Conclusion Top


Biopsy GG1 PCa is frequently upgraded after RaLRP. Using MRI as an early confirmatory test or as a treatment planning tool, we observed a 76.7% pathological upgrade at RP specimens. Patients who upgraded to GG3–5 had a shorter time to BCR than those with GG1–2. Prostate volume <30 mL and PSAD ≥0.2 ng/mL 2 measured by MRI or TRUS were significant predictive factors for biopsy GG1 upgrading. Continued effort is required for improving biomolecular and imaging strategies to classify tumor aggressiveness.

Acknowledgment

The authors appreciate the contributions of all the healthcare teams involved and all the patients enrolled in this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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  [Table 1], [Table 2], [Table 3], [Table 4]



 

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