Extended Pelvic Lymph Node Dissection during Robotic Prostate Surgery Reduces Biochemical Recurrence: A Propensity Score- matched Analysis for High-risk Prostate Cancer

doi:10.21203/rs.3.rs-1755316/v1

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Extended Pelvic Lymph Node Dissection during Robotic Prostate Surgery Reduces Biochemical Recurrence: A Propensity Score- matched Analysis for High-risk Prostate Cancer

https://doi.org/10.21203/rs.3.rs-1755316/v1

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Objectives

To avoid misunderstandings based on the failure to demonstrate oncological benefit from extended pelvic lymph node dissection (PLND) during radical prostatectomy in a recent randomized controlled trial. We evaluated early survival outcome in contemporary patients with limited to high-risk prostate cancer (PCa) using propensity score (PS)-matched analysis.

Materials and Methods

Three-hundred and forty-seven patients with high-risk PCa were enrolled. They were determined to have a lymph node (LN) involvement probability of greater than 5%. Biochemical recurrence (BCR)-free survival was compared between two groups divided by adherence with extended template and timeframe related to improving PLND procedure.

Results

The mean LN yield was 23.4 and 2.7, and the positive LN rate was 19.3 and 2.0% in the extended PLND and other groups, respectively. In the entire unmatched cohort, the estimated curve was 13.1% superior in 3-year BCR-free survival for the extended PLND group. The PS-matched cohort was converged in each LN yield group to 99 patients, and the difference in the 3-year BCR-free survival widened to 22.2% (hazard ratio 0.46, 95% confidence interval 0.27–0.80; p = 0.005). The statistical difference was consistent in standard high-risk PCa, and was a significant trend in very high-risk PCa. In the analysis of two groups divided by timeframe, the difference in the BCR-free survival was a significant trend.

Conclusion

The results possibly demonstrate the therapeutic role of extended PLND in high-risk PCa. Statistical demonstration of benefits depends on the quality of extended PLND and whether the study cohort is the optimal composition of cancer risk.

extended pelvic lymph node dissection

high-risk prostate cancer

biochemical recurrence-free survival

propensity score-matched analysis

Since 2015, prostate cancer (PCa) has become the most prevalent malignant disease in Japan and is categorized as the 6th to 7th top cause of death in Japanese men [1]. Over the last decade, radical prostatectomy has become a first-line therapy, and robotic surgery is now a standard method for patients with a localized stage PCa. Simultaneously, a paradigm shift in the surgical approach has resulted in changes to the extent or boundaries of pelvic lymph node dissection (PLND) including both better and worse results.

In the early era of minimally invasive prostatectomy done by robotic surgery, a drastically reduced rate was reported for those undergoing a PLND procedure compared to open prostatectomy. The reasons were speculated to be complicated and affected by the academic status of institutions, surgeon volume, economic issues, and regional differences [2, 3]. When viewed at a national level, this trend is still observed in Japan and in the United States [4]. In an analysis using the National Cancer Data Base, nearly 40% of patients with unfavorable risk disease did not receive PLND [5].

The recent rates for the PLND procedure and LN yield appear to have increased with improvements in safety and feasibility in proportion to the surgical volume [6]. However, there are pros and cons in systematic reviews regarding the direct benefit of PLND on oncological outcome. Even if this is the case, the majority of the results are only for biochemical recurrence (BCR)-free survival [7–10], and it is consistent that expanding the template results in more complications [11]. A long-awaited randomized controlled trial (RCT) did not demonstrate better oncological outcomes for extended PLND during radical prostatectomy, despite suggesting the potential benefits of BCR-free survival in high-grade PCa [12]. Thus, for over the last decade the therapeutic role of PLND has remained unclear.

PLND cannot be established as standard surgical management if the oncological benefit does not outweigh the negative impacts on patients. We are concerned about the current disadvantage for many high-risk PCa patients who should originally receive extended PLND solely because there is no high level of evidence. This study focused on early survival outcome, especially on BCR-free survival as an endpoint, and the therapeutic impact of extended PLND during robotic prostatectomy, which was evaluated in contemporary patients with high-risk PCa at a single-center and investigated with propensity score (PS)-matched analysis.

Patient enrollment

A total of 1,100 patients underwent robot-assisted radical prostatectomy (RARP) between October 2012 and May 2022 at our prostate center. Clinical and pathologic findings were prospectively recorded in a computer database in a stand-alone environment. Of these patients, 347 with high-risk PCa who were determined to have a LN involvement probability of greater than 5% on the Briganti 2012 nomogram were enrolled in the study [13].

National Comprehensive Cancer Network (NCCN) classification was used for entries for the entire high-risk cohort. This study applied the 2013 Johns Hopkins University criteria to stratify the entire cohort into subgroups as a standard high-risk (SHR) and very high-risk (VHR) cohort. VHR criteria were defined as multiple individual NCCN high-risk features, > 4 biopsy cores with a Gleason grade sum of 8 to 10, or a primary Gleason grade pattern 5 [14, 15].

Clinical stage in all patients was determined by assessing digital rectal examination (DRE) and multiparametric magnetic resonance imaging (MRI) findings, and the appropriate staging was used for risk stratification and nomogram. Patients diagnosed with clinically distinct positive LN (cN1), those with a total biopsy number less than 10, and those that received preoperative androgen-deprivation therapy were excluded.

Robotic prostatectomy and pelvic lymph node dissection

RARP followed by PLND was carried out using an intraperitoneal anterior approach by six surgeons, and the extended PLND template was applied from August 2015. The extended PLND template included the bilateral intrapelvic regions, such as obturator, external iliac, internal iliac, and common iliac up to the ureter crossing. Tissues in the Marcille triangle as the obturator region and lateral vesical fat tissue as the internal iliac region were included from February 2018. All our surgeons performed a mandatory self-assessment of the quality of PLND, which consisted of the degree of LN dissection in each part in the template and the reason when omitted. Prostatectomy specimens and LNs separated by regions were submitted for pathological evaluation.

Definition of BCR

BCR was defined as a prostate-specific antigen (PSA) level greater than 0.2 ng/mL with a subsequent increase, and the occurrence of BCR was the first date of confirmation. Detectable PSA greater than 0.2 ng/mL on the first checkup after surgery also followed the same criteria, and the occurrence was determined to be the date of surgery.

Grouping to compare BCR-free survival

The study endpoint was BCR-free survival as an early oncological outcome. Analysis was performed between the extended PLND group (n = 197) and the other group (n = 150) (Table 1). The other group included patients that underwent standard- (n = 23, 15.3%), limited- (n = 52, 34.7%), and omitted-PLND (n = 75, 50.0%) for following reasons; inexperienced operative technique at the early stage of robot introduction, spending time to remove adhesions in the abdominal cavity, and concerns about old age or complications of extended PLND. Considering the improvement of PLND procedure, which is an inevitable variable factor in any institutions, it seemed reasonable to analyze the timeframe instead of the cross-sectional survey, and the analysis was also performed between groups stratified according to that timeframe; before and after February 2018 (n = 128 and n = 219).

The covariate factors used in the PS-matching were age, body mass index, PSA, MRI measured prostate volume, clinical T-stage, number of biopsy cores, number of positive cores, biopsy ISUP grade groups proposed by the 2014 International Society of Urological Pathology (ISUP) [16], and Briganti LN involvement probability. In this study, the findings for multiparametric MRI were read by specialists in urologic radiology, to determine whether or not there were typical suspicious lesions for malignancy, and histopathologic specimens were evaluated by specialists in urologic pathology.

Statistical analyses

Quantitative and qualitative data were compared using Student’s t-test and a chi-squared test or Fisher’s exact, respectively. The covariate factors used at PS-matched analysis included the preoperative variables mentioned above. Survival was estimated using Kaplan–Meier analysis, and differences were compared with the log-rank test. Hazard ratios (HRs) with 95% confidence intervals (CIs) were estimated using Cox regression analysis, which was also used for conventional multivariate analyses.

All statistical analyses were performed with EZR version 1.54, which is a graphical user interface for R (2020 The R Foundation for Statistical Computing, version 4. 0. 3). All statistical tests were two-sided, with a p-value of less than 0.05 considered as statistically significant.

Pathological outcomes in high-risk entire cohort

The mean (median) LN yield in the extended PLND and the other groups was 23.4 (22) and 2.7 (1), respectively. The number (%) of patients with a positive LN was 38 (19.3) and 3 (2.0), respectively. The inequality of postoperative pathological factors such as T-stage and ISUP grade group other than the results related to LNs was resolved with an adjustment PS-matching of preoperative factors (Tables 1, 2).

BCR-free survival in high-risk entire cohort

After a mean (median) follow-up of 41.8 (36.0) months in the unmatched cohort, BCR was observed in 37 (18.8%) and 54 patients (36.0%) in the extended PLND group and the other group, respectively. The estimated curve was 13.1% (78.6 versus 65.5%, log rank p = 0.031) superior in the 3-year BCR-free survival for the extended PLND group. Median BCR-free survival was not reached in either the extended PLND and the other group (hazard ratio [HR] 0.63, 95% confidence interval [CI] 0.41–0.97; p = 0.035) (Fig. 1A).

There were some differences in preoperative factors associated with biopsy, distribution of clinical stage, and Briganti LNI probability. PS-matching was adjusted for these background differences and converged each group to 99 patients (Table 1). The difference in the 3-year BCR-free survival widened to 22.2% (82.4 versus 60.2%, log rank p = 0.004). Median BCR-free survival was not reached in either the extended PLND and the other group (HR 0.46, 95% CI 0.27–0.80; p = 0.005) (Fig. 1B).

BCR-free survival was also analyzed in the patient groups divided by statistical measures. When the entire cohort was stratified by a median LN number of 15, which corresponds to the lower limit of LN yield assessed as high quality PLND, the difference in 3-year BCR-free survival in the PS-matched cohort sustained at 18.3% (78.8 versus 60.5%, log rank p = 0.016). Median BCR-free survival was not reached in either of the LN yield groups (HR 0.52, 95% CI 0.30–0.90; p = 0.019).

BCR-free survival in high-risk subgroups

In the SHR unmatched cohort, the estimated curve showed a 13.7% advantage in 3-year BCR-free survival for the extended PLND group (84.6 versus 70.9%, log rank p = 0.017) (HR 0.49, 95% CI 0.27–0.90; p = 0.020). The PS-matched cohort was converged in each group to 73 patients, and showed a consistent statistical difference in 3-year BCR-free survival (85.7 versus 67.7%, log rank p = 0.032) (HR 0.46, 95% CI 0.22–0.96; p = 0.037) (Fig. 2A).

In the VHR unmatched cohort, 3-year BCR-free survival for the extended PLND group showed a 19.9% advantage, which was not statistically significant (65.4 versus 45.5%, log rank p = 0.140) (HR 0.64, 95% CI 0.34–1.20; p = 0.162). The PS-matched cohort was converged in each LN yield group to 22 patients, and showed a nearly significant trend for difference in 3-year BCR-free survival (76.1 versus 41.8%, log rank p = 0.084) (HR 0.46, 95% CI 0.18–1.17; p = 0.102) (Fig. 2B).

BCR-free survival in cohort stratified by timeframe

The PLND approach improved around February 2018 with a median LN yield for the extended PLND group increasing from 16 to 23. The group to be compared was mixture of patients with and without complying with the extended PLND; the extended PLND group was 21.1 and 77.6% before and after February 2018, respectively. BCR was observed in 50 (39.1%) and 41 patients (18.7%) in before and after February 2018 groups, respectively. In the unmatched cohort, the estimated curve was 8.5% superior in the 3-year BCR-free survival for after February 2018 group (76.0 versus 67.5%, log rank p = 0.147) (HR 0.73, 95% CI 0.47–1.13; p = 0.155) (Fig. 3A). In the PS-matched cohort, the difference in 3-year BCR-free survival was a significant trend at 13.3% (75.5 versus 62.2%, log rank p = 0.094) (HR 0.65, 95% CI 0.39–1.09; p = 0.103) (Fig. 3B).

Predictive postoperative factors for BCR-free survival in multivariate analysis

Conventional multivariate analysis was also performed on the model with postoperative pathological factors and PLND grouping. In addition to known pathological factors such as T-stage, N-stage, ISUP grade group, and resection margin, extended PLND was a statistically significant predictor of BCR-free survival in univariate and multivariate analyses. On the other hand, index tumor volume lost its independent value in multivariate analysis (Table 3).

Surgical parameters and complications

The mean operating time on the robotic console was 38 minutes longer (179 versus 141minutes, p < 0.001), while the mean blood loss including urine (220 versus 240mL, p = 0.250) did not increase due to the extended PLND procedure.

There were no postoperative complications classified as Clavien-Dindo grade IV or V and no statistical difference in frequency of grade III complications. There was adhesive ileus, paralytic ileus, or infectious lymphocele that required radiographic intervention or surgery in three patients of the sufficient LN yield group. There was adhesive ileus or infectious lymphocele that required radiographic intervention in two patients of the insufficient LN yield group.

This study enrolled high-risk PCa patients with estimated LN involvement of 19.4% on average. PS-matching followed by survival analysis using preoperative factors showed a statistically significant value for extended PLND with a promising hazard ratio. In addition to PS-matching, attempts to provide analyses in a cohort stratified by the median as a statistical measure and by timeframe with improved LN yield, to reduce potential bias as much as possible, also supported the existence of the oncological benefits of extended PLND. Our results of extended PLND, even when underestimated oncological benefit, outweigh the negative effects on patients and are accepted as standard surgical treatment. Furthermore, Cox regression multivariate analysis using postoperative factors showed its independent predictive value. These results potentially indicate the superiority of extended PLND for BCR-free survival and the optimal risk-range setting for patients enrolled in the study.

After safety and feasibility was established, extended PLND became the gold standard for providing accurate nodal staging [17]. Guidelines from both the American Urological Association and European Association of Urology (EAU) recommend PLND with an extended template in patients with intermediate- and high-risk PCa as an expert opinion under situations without distinct evidence of the oncological benefits of PLND [18, 19]. Some systematic reviews and meta-analysis referred to oncological outcomes, but most consisted of reports with low levels of evidence, and furthermore, there are considerable variations in the LN yield and the positive rate of metastasis [7–10]. However, recent reports found a modest superiority for PLND regarding the effects of BCR-free survival with hazard risks of approximately 0.6–0.7 [8, 9].

The first attempt of a RCT to determine the oncological benefit of extended PLND unfortunately failed to show a statistically significant difference, despite the study being precisely designed to expect a 15% advantage in BCR-free survival [12]. The report is an important reference in the field of PLND. However, as pointed out in correspondence, there was a favorable cancer profile characterized by more than one-third of patients having an ISUP grade group 1, and the estimated risk of LN involvement was 11 to 12%, which might be due to incorrect patient selection that reduced the effect of extended PLND [20]. On the contrary, a recent RCT to determine the role of prophylactic pelvic irradiation for high-risk, locally advanced PCa successfully showed improved disease-free survival [21]. Although one cannot compare the different treatment modalities on the same basis, the crucial difference between them is that the enrolled patients had a higher risk PCa in the latter RCT; the estimated risk of LN involvement was more than 20%. Therefore, strategic planning prior to a study is essential for risk-range setting or optimal composition of cancer risk regardless of study design, especially when shedding light on demonstrating the therapeutic role of PLND. In this sense, the composition of PCa patients who entered this study might have been appropriate.

In interpreting this study, it is necessary to understand the unique characteristics. The current study enrolled PCa patients whose clinical stage had been determined by a combination of DRE and multiparametric MRI. The use of an MRI finding leads to a significant upstaging of clinical T-stage and risk grouping, and further affects treatment intensification in around 30% of patients. These effects arise as MRI shows higher sensitivity and lower specificity compared to DRE [22]. Recent reports suggest that MRI staging has advantages in the established risk grouping, i.e., EAU risk group, and LN involvement nomograms, i.e., Memorial Sloan Kettering Cancer Centre 2018 and Briganti 2012 nomograms, which were originally developed by DRE staging [23, 24].

Whereas, in our cohort, the re-classification to high-risk from intermediate-risk was less than 5%, and to VHR from the SHR subgroup was around 20.0%. For all, the risk migration remained less than 10%. This is probably because the staging did not rely solely on MRI, and the NCCN classification with T3 or higher as one of the high-risk criteria was used in the risk stratification. Actually, the concordance rate between MRI and DRE was high in determining clinical T3 stage in our cohort. Nevertheless, the measured values of BCR-free survival cannot merely be compared to those in other reports since the Will Rogers phenomenon arising from the risk migration has occurred often [25].

A recent report using causal mediation analysis indicated that the impact of extended PLND was not restricted to a staging benefit, but also involved a therapeutic benefit of reducing BCR or second-line therapy experience at approximately 30% [26]. A statistical approach using the rigorous application of a causal inference framework and the concept of causal mediation analysis is frequently used analysis in the field of psychology, but its effectiveness as an analytical method in the field of oncology is still immature. Although it has traditionally been considered desirable that the type of study investigating the therapeutic effect of PLND be determined by RCT, when a well-designed RCT is not feasible due to ethical issues, such methodology may provide hints for solving analytical challenges for exploring oncological benefits of PLND.

There are some limitations to our study. Although, data were collected prospectively the study design is a retrospective analysis, short follow-up periods, and the small number of patients would limit the oncological impact of the results. Even PS-matching adjusted for differences in known background factors will not remove all of the thinly veiled bias. Despite such limitations, this report should serve as a reference indicating the positive therapeutic role of extended PLND.

There should be PCa patient benefit from PLND that is performed with the extended template and removal of a sufficient number of LNs. Our study potentially demonstrates the therapeutic role of PLND in high-risk PCa that may harbor both recognizable and unrecognizable metastases. Demonstration of therapeutic benefit of extended PLND depends on its quality, and whether the study cohort is the optimal composition of cancer risk regardless of study design.

Funding: None

Competing Interests: The authors declare that they have no competing interests.

Authors' contributions:

Masahiro Yashi, Megumi Yokoyama, and Takao Kamai initiated this study, participated in its design and coordination, carried out the study and drafted the manuscript. Gaku Nakamura, Toshitaka Uematsu, Issei Suzuki, Kazumasa Sakamoto, and Daisaku Nishihara performed the statistical analysis. Masahiro Yashi, Issei Suzuki, and Toshiki Kijima were surgeons of robot-assisted radical prostatectomy and carried out the study. Kazuyuki Ishida and Yasushi Kaji were uropathologist and uroradiologist, respectively, and advised the manuscript design. All authors read and approved the final manuscript.

Acknowledgement:

The authors are special thanks to Toshimi Sairenchi, Chief director of Center for Research Collaboration and Support in Comprehensive Research Facilities for Advanced Medical Science at Dokkyo Medical University for his statistical advice in conducting this study.

Ethics and patient consents

This study was conducted in accordance with the Helsinki Declaration and was approved by the institutional ethical review boards at Dokkyo Medical University Hospital: Approval number #28010 including the responsibility to report the results of this study for further clinical evaluation. In addition, each patient signed an informed consent form regarding the storage of their information for the purpose of research and acknowledged that the results of this study did not affect the subsequent clinical course.

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Table 1-3 are available in the Supplemental Files section.

No competing interests reported.

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Extended Pelvic Lymph Node Dissection during Robotic Prostate Surgery Reduces Biochemical Recurrence: A Propensity Score- matched Analysis for High-risk Prostate Cancer

Status:

Version 1

Abstract

Objectives

Materials and Methods

Results

Conclusion

Figures

Background

Methods

Patient enrollment

Robotic prostatectomy and pelvic lymph node dissection

Definition of BCR

Grouping to compare BCR-free survival

Statistical analyses

Results

Pathological outcomes in high-risk entire cohort

BCR-free survival in high-risk entire cohort

BCR-free survival in high-risk subgroups

BCR-free survival in cohort stratified by timeframe

Predictive postoperative factors for BCR-free survival in multivariate analysis

Surgical parameters and complications

Discussion

Conclusion

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1