Transperineal biopsy is associated with higher rates of Gleason grade group upgrading in prostate adenocarcinoma when compared with transrectal ultrasound biopsy

doi:10.21203/rs.3.rs-5209105/v1

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Research Article

Transperineal biopsy is associated with higher rates of Gleason grade group upgrading in prostate adenocarcinoma when compared with transrectal ultrasound biopsy

https://doi.org/10.21203/rs.3.rs-5209105/v1

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Purpose:

Histopathological assessment of prostate biopsies (PBx) remains the mainstay of diagnosis in prostate cancer (PCa). The Gleason grade group score (GGG) is a critical parameter used for diagnosis, risk stratification and management in PCa. In our institution transperineal (TP) PBx has become the favoured biopsy method, largely due to its increased accuracy and lower risk of infection. Our review analysed the GGG concordance rates between PBx and radical prostatectomy (RP) specimens with a focus on biopsy method.

Method:

A total of 588 patients who underwent RP between January 2016 and December 2022 were included in our analysis. Clinicopathological data was collected from the laboratory information system. A chi-square and Mann-Whitney U test were used for categorical and continuous variables, respectively.

Results:

TRUS biopsy was performed in 79% of cases, while TP PBx was performed in 21%. Concordance between PBx and RP was observed in 58% of cases, with 22% being upgraded and 20% downgraded. Biopsy method, extra-prostatic extension and positive surgical margin status were all found to be significantly associated with GGG upgrading.

Conclusion:

TP biopsies is the favoured biopsy method in our institution and review reveals higher rates of GGG upgrading is associated with this approach. This presents a dilemma as TP PBx may compromise the precision of cancer grading in favour of reduced side effects. Ongoing monitoring of PBx and their outcomes is essential for optimal balance between diagnostic accuracy and procedure side effects.

Prostate Cancer

Gleason Grade Group

Transperineal Biopsy

Transrectal Biopsy

Prostate cancer (PCa) is the most common non-cutaneous invasive cancer affecting men both in Ireland and internationally. [1, 2] The disease causes significant morbidity and mortality with an estimated 299,010 new cases in the United States in 2024 and an estimated death toll of 35,250 from the condition. [3]

The histological assessment of prostate tissue remains the mainstay of diagnosis of PCa. [4] In addition to a cancer diagnosis, prostate biopsies (PBx) are pathologically risk stratified using the Gleason score (GS), and more recently the Gleason Grade Group (GGG) system. [5] This pathological grading has a significant impact on the management of PCa patients and its accuracy is of the upmost importance to urologists. [6] Unfortunately discordance rates between the GGG assigned at PBx and those assigned at radical prostatectomy (RP) are high, with some studies reporting discordance rates to be as high as 62.8% and 45.4% [7, 8]. GGG upgrading occurs when a GGG is found to be higher in the surgical specimen when compared with the PBx, and this is associated with worse outcomes for the patient. [9, 10]

Transperineal (TP)-guided biopsy has increasingly become the biopsy method of choice in recent years. When compared with transrectal ultrasound (TRUS)-guided biopsy, TP is more effective at detecting tumours in the apex and anterior aspect of the prostate. [11, 12] Moreover, the TP-guided method is significantly associated with a lower risk of infection and sepsis. [12, 13] This shift in biopsy technique aims to both minimises patient risk and improving diagnostic accuracy.

Despite a change in biopsy method, the high rate of discordance between biopsy and post-surgical pathology remains a critical issue in PCa. Accurate Gleason grading is crucial for determining the risk stratum and appropriate treatment plan, which can range from active surveillance to radical interventions such as RP. Misgrading may lead to overtreatment, causing unnecessary side effects, or alternatively undertreatment, leaving the patient at risk of disease progression. Therefore, understanding the factors that contribute to grading discordance is vital for improving patient outcomes.

In our study we aimed to review if biopsy technique impacted GGG concordance rates in our institution and examine for any variables that may help predict pathological discordance between PBx to RP. By identifying these variables, we hope to enhance the predictive accuracy of our diagnostic biopsies and in turn optimise treatment strategies for PCa patients. This study looks to provide valuable insights into how biopsy techniques and other factors are influencing diagnostic accuracy and patient management.

Study Design and Population

We performed a retrospective cohort analysis to investigate if the method of PBx impacted GGG concordance rates. The study was performed at St Vincent’s University Hospital (SVUH) and included patients who were coded as having undergone a RP between 01/01/2016 and 31/12/2022 (n = 830). The study was approved by the Department of Clinical Audit, SVUH ethical approval was not required as all patient data was anonymised. The study population consisted of patients who underwent a RP in SVUH and had either a TRUS-guided biopsy or a TP-guided biopsy prior to surgery. Patients were excluded if an alternative diagnosis was provided in the surgical histology report, an alternative procedure to a RP was performed, no biopsy histology was available, histology reports were incomplete or if previous radiotherapy or hormone therapy was received. A total of 588 patients met the inclusion criteria and were included in the final analysis.

Data Collection & Outcome Measures

Data was collected retrospectively from the laboratory information system in SVUH. The primary exposure variables extracted were the method of biopsy, categorised as TRUS or TP biopsy, the highest GGG assigned in any one core PBx and the highest GGG assigned to the RP. Further data extracted included demographic information (age) and histopathological outcomes (the presence of positive surgical margins, extra-prostatic extension (EPE), seminal vesicle involvement (SVI), and lymph node involvement). The primary outcome was concordance between the GGG assigned to the PBx and the GGG assigned to the RP and whether there was a distinction between the biopsy methods. Secondary outcomes included assessment of the histopathological features as listed above and their relationship to GGG concordance rates. Data was anonymised to protect patient privacy.

Statistical Analysis

Descriptive statistics were used to summarize the baseline characteristics of the study population. Continuous variables were presented as medians and interquartile ranges, as appropriate. Categorical variables were presented as frequencies and percentages. Comparative analyses were performed using the Mann-Whitney U test for continuous variables and the chi-square test for categorical variables. The results were presented using confidence intervals (CIs) and a p-value of less than 0.05 was considered statistically significant. All statistical analyses were performed using Microsoft Excel version 16.86 (24060916).

Between January 2016 and December 2022, 830 patients were coded as having underwent a RP at SVUH. Two hundred and forty-two of these patients were excluded from the study on the basis of miscoding (n = 100) (e.g., benign prostatic hyperplasia), an incorrect procedure code was used (n = 77), no biopsy histology reports were available (n = 40), the histopathology report was incomplete (n = 24), and there was a single patient excluded for having received androgen and radiotherapy treatments prior to RP, which might affect the histology of their RP specimens. A total of 588 patients with completed histopathology data of both their PBx and RP specimens were included in the current study.

Table I shows the demographic and clinical information of the patients in this study. The median age at RP was 63 years [interquartile range (IQR) = 63–66]. TRUS-guided biopsy was the method of diagnosis for 79% of patients, while 21% were diagnosed via TP-guided biopsy. Over the six-year period TP-guided biopsy gradually became the biopsy method of choice in SVUH. Initially this biopsy method accounted for 0% of the patients who proceeded to RP in 2016. Over the next six-year period (2017–2022) it would account for 2%, 7%, 10%, 14%, 29% and 55% of cases respectively. An increase in the number of RP performed at SVUH was also noted over the seven-year period, with the number increasing from 48 in 2016 to 119 in 2022. The final pathological stage of all cases was pT2 in 65% of cases, pT3a in 25% of cases with the remaining 10% of cases categorised as pT3b. Extra-prostatic extension was present in 33% of cases, a positive surgical margin in 22% of cases and seminal vesicle involvement in 10% of cases. Thirty-six percent of cases had lymph node sampling of which 8% of these cases were positive for lymph node metastasis.

Table I

Clinicopathological characteristics of study population

Characteristic	n(%)	n(%)	n(%)
Age at diagnosis (yr)
Median (IQR)	63(63–66)
	Method of diagnosis
	TRUS	TP	Total
Total RP	463 (79)	125 (21)	588 (100)
Year of RP
2016	48 (100)	0 (0.0)	48 (100)
2017	58 (98.3)	1 (1.7)	59 (100)
2018	77 (92.7)	6 (7.3)	83 (100)
2019	74 (90.2)	8 (9.8)	82 (100)
2020	75 (86.2)	12 (13.8)	87 (100)
2021	78 (70.9)	32 (29.1)	110 (100)
2022	53 (44.5)	66 (55.5)	119 (100)
Pathological Stage
pT2	348 (65.2)
pT3a	133 (24.9)
pT3b	52 (9.8)
EPE status
Negative	392 (66.6)
Positive	196 (33.3)
Surgical Margin Status
Negative	460 (78.2)
Positive	128 (21.8)
SVI Status
Negative	531 (90.3)
Positive	57 (9.7)
Lymph Node Status
Cases not sampled	375 (63.7)
Cases sampled	213 (36.3)
Of cases sampled
Negative	195 (91.5)
Positive	18 (8.5)
Note: IQR = Interquartile Range, RP = Radical Prostatectomy, TRUS = Transrectal ultrasound, TP = Transperineal, EPE = Extra-prostatic extension, SVI = Seminal Vesicle Involvement

Table II shows the change in GGG assigned at RP stratified by the GGG assigned at PBx. For the GGG reported for the RP specimen 342 (58%) were unchanged when compared with the GGG assigned at PBx i.e. concordant, while 116 (20%) were downgraded and 129 (22%) were upgraded. On review of the individual grade groups, the most frequent upgrading occurred in men with GGG 1 on PBx who were upgraded in 48% of cases, mainly into GGG 2 which accounted for 83% of these upgraded cases. Downgrading was most frequently seen in men with GGG 4 and GGG 3 on PBx with 55% and 37% of these downgraded respectively. Of the five GGGs, GGG 4 and GGG 3 were the least predictive of the final GGG at RP.

Table II

Gleason Grade Groups of PBx and RP specimens

Biopsy Gleason Groups	RP Specimens Gleason Grade Groups, n(%)
Biopsy Gleason Groups	1 (6)	2 (3 + 4)	3 (4 + 3)	4 (8)	5 (9&10)	Total
1 (6)	49 (52.1)	40 (42.5)	2 (2.1)	3 (3.2)	0 (0.0)	94 (100)
2 (3 + 4)	12 (6.0)	153 (76.8)	21 (10.5)	9 (4.5)	4 (2.0)	199 (100)
3 (4 + 3)	0 (0.0)	37 (29.6)	55 (44.0)	21 (16.8)	12 (9.6)	125 (100)
4 (8)	0 (0.0)	15 (14.1)	40 (37.7)	34 (32.0)	17 (16.0)	106 (100)
5 (9&10)	1 (1.5)	8 (12.5)	4 (6.2)	51 (79.6)	0 (0.0)	64 (100)
Total	62 (10.5)	253 (43.0)	122 (20.7)	118 (20.0)	33 (5.6)	588 (100)
Note: PBx = Prostate Biopsy, RP = Radical Prostatectomy

Table III shows the characteristics of patients who have concordant or upgraded GGG. TP was found to be significantly associated with GGG upgrading. EPE and SVI were also found to be significantly associated with GG upgrading. Although a positive surgical margin status was not found to be statistically significant in our analysis it was more frequently associated with GGG upgrading.

Characteristic	Concordant (n = 342)	Upgraded (n = 129)	p
Age at diagnosis	61.4	61.8	0.047
Biopsy Method
TRUS	273 (79.8)	89 (68.9)	0.01
TP	69 (20.2)	40 (30.1)
EPE Status
Positive	102 (29.8)	59 (45.7)	0.001
Negative	240 (70.2)	70 (54.2)
Surgical margin status
Positive	72 (21.1)	31 (24.0)	0.49
Negative	270 (78.9)	98 (76.0)
SVI Status
Positive	26 (7.6)	20 (15.5)	0.001
Negative	316 (92.4)	109 (84.5)
Data presented as n(%)
Table III

Characteristics of patients with concordant and upgraded Gleason groups

In keeping with current literature, our study reinforces one of the key challenges in the risk stratification of PCa patients: the notable high discordance rates between the GGG assigned at PBx and RP. [9–11] We found a concordance rate of 58% in our population, with 20% of our cases being downgraded and 22% of our cases being upgraded. Several factors may contribute to this discordance. Interobserver variability between reporting pathologists is well recognised and is likely a significant factor. [14] While this is minimised in our department, with a select number of consultant histopathologists reporting PBx, variation cannot be eliminated entirely. Additionally, sampling error due to tumour heterogeneity is likely a contributory factor. Prostate tumours often contain multiple Gleason grades within the same tumour and the specific area biopsied may not reflect the highest Gleason grade present in that tumour. [15] Furthermore, PCa may not only be heterogeneous but may contain multiple foci of PCa, with one study finding two or more adenocarcinomas in 87% of their RP specimens. [16] Although MRI targeted biopsies and extensive prostate sampling aim to reduce this issue, it likely still contributes to discordance.

In 2016 none of the patients who underwent a RP in SVUH had a TP PBx as their diagnostic biopsy method. Our study offers real-world data illustrating the trend shift from TRUS PBx to TP PBx over a seven-year period, rising annually with TP biopsies ultimately accounting for 55% of patients who underwent a RP in our institution. No significant difference was found in the overall concordance rates between TP PBx (55%) and TRUS PBx (59%) in our cohort and this is reflective of the findings presented in the literature by Evans et al and Uleri et al [10, 17]. However, when examining upgrading in isolation, our study diverged from the findings of Evans, Qu and Scott et al, who reported lower rates of upgrading following TP biopsies. [10, 18, 19] In contrast to their findings, our data indicates that while overall concordance rates were similar, there was a significant association between upgrading and TP biopsies (p = < 0.01). This finding is clinically significant, as upgrading at RP is associated with poorer outcomes. [20] A potential explanation for this observation is that those deemed clinically lower-risk patients with normal MRIs are more likely to be selected for TP biopsy over TRUS biopsy, possibly contributing to the higher observed rate of upgrading at RP.

Our study also found a significant association of both EPE (p = 0.001) and SVI (p = 0.001) with GGG upgrading at RP. These finding align with previous research highlighting that EPE and SVI are predictors of worse outcomes and as such are factors that upstage a tumour to pT3a & pT3b in the TNM classification system respectively. [20, 21] Moreover, EPE and a positive surgical margin status have been significantly associated with early biochemical recurrence in patients who have undergone RP [22, 23] and while a positive surgical margin status (103/471) did not reach statistical significant in our study it was observed more frequently in RP specimens that were upgraded. These observations are relevant for both clinicians and histopathologists. For clinicians the presence of these histological features may signal a more aggressive disease and as such help inform post-operative management and decision making around adjuvant therapy. [24] For histopathologists the identification of adverse pathological features should prompt increased vigilance when assigning GGG to RP specimens given such features are associated with higher GGG. [25, 26]

Our study has several strengths. The large sample size of 588 patients provides a robust data set for analysis. Additionally, the trend analysis documenting the shift in biopsy techniques over seven years offers valuable insights into evolving clinical practices. The detailed assessment of multiple pathological outcomes, including GGG concordance and adverse pathological features, provides a comprehensive view of the factors influencing grading discordance. However, there are notable limitations to our work. Firstly, the retrospective nature of the study may introduce selection bias and limit the ability to establish causal relationships. Secondly, the study’s findings are based on data from a single institution, which again adds to the selection bias and lack of variability in work practices. Thirdly, we did not perform multivariable regression analyses to adjust for potential confounders, which may affect the validity of our findings. Lastly, sensitivity analyses were not conducted to assess the robustness of our results. These limitations should be considered when interpreting the results of this study.

In conclusion, our study highlights the ongoing challenge in accurately predicting final pathological outcomes for PCa patients from initial biopsy results. Despite the increasing adoption of TP-guided biopsies, we found no significant difference in overall GGG concordance rates between TP and TRUS biopsies. However, TP biopsies were significantly associated with GGG upgrading, which has important clinical implications. Our findings support the need for continued efforts to improve PCa risk stratification.

Author Contribution

Paul Reddy undertook the data collection, performed the statistical analysis, prepared figures and wrote the main manuscript text.Niall Swan oversaw the project from start to finish reviewing the initial data, draft abstracts and reviewed the manuscript providing comments and edits. David Galvin reviewed initial data, draft abstracts and the manuscript, providing comments and edits.Robert A. Keenan and Tom Crotty reviewed the manuscript and provided comments and edits.

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No competing interests reported.

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You are reading this latest preprint version

Transperineal biopsy is associated with higher rates of Gleason grade group upgrading in prostate adenocarcinoma when compared with transrectal ultrasound biopsy

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Abstract

Introduction

Methods and Materials

Study Design and Population

Data Collection & Outcome Measures

Statistical Analysis

Results

Discussion

Declarations

Author Contribution

References

Additional Declarations

Status:

Version 1