Perioperative outcomes and postoperative functional outcomes of robot-assisted radical prostatectomy for oligometastatic versus localized prostate cancer: a multicenter matched case-control study

Introduction

The concept of “oligometastasis” was first proposed by Hellman and Weichselbaum in 1995 (1). The current consensus definition for oligometastatic prostate cancer (OmPCa) is the presence of 1–5 metastatic lesions confined to the bone and/or lymph nodes, excluding visceral metastases. This disease state is considered an intermediate stage between localized disease and widespread metastasis (2), with the potential for clinical cure (3). According to the 2025 European Association of Urology (EAU) guidelines, the standard first-line treatment for OmPCa is androgen deprivation therapy (ADT) combined with chemotherapy or radiotherapy (4,5); however, their effectiveness in delaying disease progression and prolonging survival remains limited.

With the deepening understanding of tumor biology, multiple studies have confirmed that surgical resection of the primary tumor in metastatic disease can significantly improve patient prognosis, with some cases even achieving clinical cure (6-8). On this basis, the therapeutic scope of radical prostatectomy (RP) has been extended to OmPCa, and related explorations aim to evaluate its potential to improve patient survival outcomes (9-11). The most classic and well-established indication for RP is localized prostate cancer (LPCa), for which perioperative risks have been well defined. However, compared with LPCa, OmPCa patients typically have higher Gleason scores, higher prostate-specific antigen (PSA) levels, and more advanced clinical T stages, which may theoretically increase surgical difficulty, risk of neurovascular bundle (NVB) invasion, and perioperative complication rates. The safety and feasibility of RP in OmPCa patients still require further evidence-based medical support.

Therefore, based on multicenter clinical data, this study systematically evaluates the safety and feasibility of robotic-assisted radical prostatectomy (RARP) in OmPCa patients by comparing perioperative outcomes, as well as postoperative functional outcomes such as erectile function and urinary continence, between OmPCa and LPCa patients. The aim is to provide new clinical evidence for the rational application of this procedure in the treatment of OmPCa. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-aw-527/rc).

Methods

Study population

This study employed a multicenter retrospective case-control design. Electronic medical records of prostate cancer (PCa) patients who underwent RARP between March 2010 and December 2023 at the urology departments of five tertiary hospital centers in China (The First, Third, Sixth Medical Centers of Chinese PLA General Hospital, the First Affiliated Hospital of Nanchang University and the First Affiliated Hospital of Soochow University). Among these, 100 OmPCa patients met all inclusion and exclusion criteria. To rigorously control for selection bias between groups, 100 LPCa patients were 1:1 matched based on surgical center and operative date using a case-matching method. The screening and matching flowchart is presented in Figure 1.

Figure 1 The screening and matching flowchart. LPCa, localized prostate cancer; MRI, magnetic resonance imaging; NVB, neurovascular bundle; OmPCa, oligometastatic prostate cancer; PET/CT, positron emission tomography/computed tomography; RARP, robotic-assisted radical prostatectomy; RP, radical prostatectomy; TURP, transurethral resection of the prostate.

This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The protocol was approved by the Ethics Committee of Chinese PLA General Hospital (No. S2025-406-01), The First Affiliated Hospital of Nanchang University (No. IIT-2024-657) and The First Affiliated Hospital of Soochow University (No. 2026-198). All eligible patients provided written informed consent. All participating hospitals were informed and agreed on the study.

Inclusion criteria: (I) postoperative pathological diagnosis of PCa; (II) both magnetic resonance imaging (MRI) and positron emission tomography/computed tomography (PET/CT) results showing ≤5 bone and/or distant lymph node metastases, defining OmPCa; (III) MRI results showing no lymph node and/or distant metastasis, defining LPCa; (IV) underwent RARP without preservation of the bilateral NVB after definitive diagnosis, with all surgeries performed by senior surgeons at or above the rank of associate chief physician who had surpassed the learning curve for the procedure; (V) primary cases. Exclusion criteria: (I) MRI and PET/CT results showing >5 bone and/or lymph node metastases, or detection of visceral metastases; (II) patients who underwent open RP or laparoscopic RP after definitive diagnosis, or who did not undergo surgical treatment; (III) patients with concomitant tumours; (IV) patients who underwent transurethral resection of the prostate (TURP); (V) patients with incomplete clinical data.

Observation indicators

(I) Perioperative outcomes including surgical duration, intraoperative blood loss, intraoperative blood transfusion volume, postoperative hospital stay, postoperative 24-hour drainage volume, total postoperative drainage volume, and postoperative drainage tube retention time, and postoperative urinary catheter retention time, etc. A consistent protocol for perioperative outcomes was adopted across all centers. Surgical duration was defined as the duration from skin-to-skin. The discharge criterion was patient tolerance of a liquid diet and removal of all drainage tubes, with tube removal itself requiring drainage fluid to appear clear and measure <50 mL/day. (II) Positive surgical margin (PSM) status. PSM is defined as the presence of malignant glandular structures at the ink-stained surgical margin of the specimen. All sections are reviewed histologically by experienced urogenital pathologists. (III) Perioperative complications, including infection, anastomotic leakage, intestinal injury or obstruction, lymphatic leakage, etc., are recorded according to the Clavien-Dindo classification system within 30 days. (IV) Functional outcomes were assessed using a composite evaluation method. Postoperative urinary continence was evaluated by the number of daily pads used and the urinary incontinence (UI) domain of the Expanded Prostate Cancer Index Composite-26 (EPIC-26) questionnaire. Postoperative erectile function was assessed using the International Index of Erectile Function-5 (IIEF-5) score and the sexual domain of the EPIC-26 questionnaire. UI was defined as the use of ≥1 pad per day. Erectile dysfunction (ED) was defined as an IIEF-5 score ≤16, with or without the use of oral phosphodiesterase type 5 inhibitors (PDE5i). All EPIC-26 domain scores were calculated according to established guidelines, ranging from 0 to 100, with higher scores indicating better function. The reporting of EPIC-26 scores was supplemented by referencing established minimal clinically important difference (MCID) thresholds for patient-reported outcome measures, with MCID set at 10 points for the sexual domain and 6 points for the UI domain.

Data were collected at baseline (preoperatively), 3 months, and 12 months postoperatively to assess postoperative urinary continence, erectile function, and complications. All assessments of perioperative outcomes, functional outcomes, and related complications were conducted by independent research nurses not involved in patient care. They used a standardized follow-up checklist (including the aforementioned questionnaires) administered via outpatient visits or telephone interviews.

Statistical analysis

Statistical analyses were performed using SPSS software (version 25.0). Normally distributed quantitative data were presented as mean ± standard deviation (SD) and analyzed using the Student’s t-test. Non-normally distributed quantitative data were presented as medians [interquartile ranges (IQRs)] and analyzed using the Mann-Whitney U test. Qualitative data were presented as frequencies (%) and analyzed using the χ² test. All tests were two-sided, with a significance level (α) set at 0.05. A P value <0.05 was considered statistically significant.

To evaluate changes in EPIC-26 scores over time while accounting for the correlation among repeated measures, separate generalized estimating equation (GEE) models were fitted for scores from the UI and sexual function domains as dependent variables. Each model included group, time, and their interaction term.

Results

Baseline patient characteristics

The OmPCa group and the LPCa group enrolled 100 patients each. The OmPCa group demonstrated significantly higher preoperative PSA levels, biopsy Gleason scores, and clinical T stages compared to the LPCa group (all P<0.05). No statistically significant differences were observed in other baseline characteristics, including age, body mass index (BMI), prostate volume, and seminal vesicle invasion status (all P>0.05), as detailed in Table 1.

Preoperative neoadjuvant endocrine therapy was administered to 25 (25.0%) and 11 (11.0%) patients in the OmPCa and LPCa groups, respectively. According to guideline recommendations (12), pelvic lymph node dissection (PLND) was performed in 33 (33.0%) and 6 (6.0%) patients in the OmPCa and LPCa groups, respectively. These differences were statistically significant (both P<0.05).

Surgical and postoperative pathological information

The median operative times were 154 (IQR, 120, 185) minutes in the OmPCa group and 150 (IQR, 120, 175) minutes in the LPCa group. The median postoperative hospital stay was 5 (IQR, 4, 7) days and 4 (IQR, 4, 5) days, respectively. The median 24-hour postoperative drainage volume was 120 (IQR, 76, 179) mL in the OmPCa group and 128 (IQR, 100, 150) mL in the LPCa group. The median total postoperative drainage volume was 195 (IQR, 136, 410) mL and 185 (IQR, 122, 335) mL, respectively. The median intraoperative blood loss was 100 (IQR, 100, 50) mL in both groups. The median duration of postoperative drain indwelling was 3 (IQR, 2, 4) days in the OmPCa group and 3 (IQR, 3, 3) days in the LPCa group. The median duration of urinary catheter indwelling was 14 (IQR, 14, 14) days in both groups. No patients in either group required an intraoperative blood transfusion. None of these differences between the groups were statistically significant (all P>0.05), as detailed in Table 2.

Postoperative pathological results revealed PSM in 35.0% (35/100) of the OmPCa group and 30.0% (30/100) of the LPCa group, with no statistically significant difference (P=0.45).

Postoperative complications within 30 days, assessed using the Clavien-Dindo classification system, were as follows: in the OmPCa group, one patient experienced pelvic effusion (Grade IIIa), one had a rectal injury (Grade II), one developed a urinary tract infection (Grade II), and one presented with chylous leakage (Grade I). In the LPCa group, one patient experienced ureteral stenosis (Grade IIIb), and one had anastomotic leakage (Grade IIIa). The overall complication rates were not significantly different between the OmPCa and LPCa groups (4.0% vs. 2.0%, P=0.41).

Postoperative urinary continence outcomes

Regarding the evaluation of urinary continence function, all 200 patients completed the baseline, 3 months, and 12 months postoperative follow-up assessments. The two groups demonstrated similar baseline scores in the EPIC UI domain [100.0 (IQR, 93.8, 100.0) vs. 100.0 (IQR, 93.8, 100.0), P=0.55; Figure 2A and Table 3]. From baseline to 12 months postoperatively, the mean change in the UI score was −22.0 points [95% confidence interval (CI): −25.1 to −18.9] in the OmPCa group and −22.1 points (95% CI: −25.3 to −19.0) in the LPCa group, both representing significant declines from baseline (all P<0.001). Notably, the magnitude of change exceeded the established MCID for the incontinence domain. However, no statistically significant intergroup differences were observed in the UI domain scores at either the 3 months [62.5 (IQR, 56.3, 67.2) vs. 56.3 (IQR, 50.0, 62.5), P=0.21; Figure 2A and Table 3] or 12 months [75.0 (IQR, 62.5, 85.9) vs. 75.0 (IQR, 62.5, 87.5), P=0.83; Figure 2 and Table 3] postoperative assessments. Furthermore, the proportion of patients reporting a score decline greater than the MCID at 12 months relative to baseline did not differ significantly between groups (76% vs. 67%, P=0.16).

Figure 2 Mean EPIC-26 domain scores in two groups of patients: (A) urinary incontinence domain scores; (B) sexual domain scores. EPIC-26, Expanded Prostate Cancer Index Composite-26; LPCa, localized prostate cancer; OmPCa, oligometastatic prostate cancer; RARP, robotic-assisted radical prostatectomy.

GEE analysis revealed a non-significant main effect for group (Wald χ²=0.02, P=0.90), indicating no overall difference in EPIC UI scores between the OmPCa and LPCa groups. A significant main effect for time was identified (Wald χ²=1,986.93, P<0.001), reflecting a substantial improvement in incontinence scores over time in both groups. Crucially, the group × time interaction effect was not statistically significant (Wald χ²=2.49, P=0.29), suggesting that the trajectory or rate of change in UI scores did not differ between the two groups.

No patients in either group presented with preoperative UI. The urinary continence recovery rates in the OmPCa and LPCa groups at 1 month (57.0% vs. 60.0%, P=0.67), 3 months (74.0% vs. 78.0%, P=0.51), and 12 months (86.0% vs. 89.0%, P=0.52) postoperatively showed no statistically significant differences. GEE analysis confirmed a non-significant main effect for group (Wald χ²=0.33, P=0.57), denoting no overall disparity in UI recovery rates. A significant main effect for time was again observed (Wald χ²=70.14, P<0.001), consistent with progressive recovery over time in both groups. The group × time interaction effect remained non-significant (Wald χ²=0.18, P=0.91), indicating comparable recovery trajectories between the groups, as shown in Figure 3.

Figure 3 The postoperative urinary continence recovery rate in two groups of patients. LPCa, localized prostate cancer; OmPCa, oligometastatic prostate cancer.

Postoperative sexual function outcomes

For the evaluation of erectile function, all 200 patients completed the baseline, 3 months, and 12 months postoperative follow-ups. Baseline scores in the EPIC sexual domain were comparable between groups [62.5 (41.7, 79.2) vs. 62.5 (41.7, 79.2), P=0.94; Table 3]. From baseline to 12 months post-surgery, the mean change in the sexual score was −46.1 points (95% CI: −49.6 to −42.6) for the OmPCa group and −39.0 points (95% CI: −44.0 to −34.0) for the LPCa group, both indicating significant deterioration from baseline (all P<0.001) that surpassed the MCID for the sexual domain. In contrast to the sexual function outcomes, statistically significant differences in sexual domain scores were evident between groups at both 3 months [12.5 (5.2, 20.8) vs. 16.7 (8.3, 25.0), P=0.03; Table 3] and 12 months [16.7 (8.3, 20.8) vs. 22.9 (12.5, 33.3), P<0.001; Table 3] postoperatively. Moreover, the proportion of patients experiencing a score decline greater than the MCID at 12 months relative to baseline differed significantly (100% vs. 83%, P<0.001).

GEE analysis yielded a significant main effect for group (Wald χ²=4.60, P=0.03), signifying an overall difference in EPIC sexual function scores between the OmPCa and LPCa groups. The main effect for time was also significant (Wald χ²=1,124.55, P<0.001), denoting marked temporal changes in scores within both cohorts. Importantly, the group × time interaction effect reached statistical significance (Wald χ²=53.78, P<0.001), implying divergent trajectories in the rate of sexual function score change between the two groups (see Figure 2).

After excluding 18 and 20 patients with pre-existing ED from the OmPCa and LPCa groups, respectively, 82 and 80 patients were included in the ED-specific analysis. At the 1-year postoperative follow-up, the incidence of postoperative ED was significantly higher in the OmPCa group than in the LPCa group (95.1% vs. 81.3%, P=0.006).

Discussion

In recent years, as the mechanisms by which primary tumors mediate the metastatic process and promote the formation of distant metastases through circulating tumor cells have been gradually elucidated (13), performing RP for OmPCa has increasingly become a research focus. Existing studies have preliminarily confirmed the safety and feasibility of RP for OmPCa (14), but these studies generally had small sample sizes and were based on open or laparoscopic surgery. With the continuous maturation and refinement of robot-assisted surgical technology, RARP has gradually become the mainstream surgical approach for RP, owing to its advantages such as reduced intraoperative blood loss, faster postoperative recovery, higher rates of functional preservation, and lower risk of complications (15). Therefore, this study aims to evaluate the safety and feasibility of RARP in patients with OmPCa.

To the best of our knowledge, this study is the first multicenter clinical investigation to evaluate RARP for the treatment of OmPCa. We compared the baseline characteristics, perioperative outcomes, and postoperative functional outcomes between the OmPCa group and the LPCa group. Although OmPCa patients typically have a higher tumor burden, with significantly higher preoperative PSA levels, biopsy Gleason scores, and clinical T stages than the LPCa group (all P<0.05), our results showed no significant differences in perioperative outcomes between the two groups, including operative time, intraoperative blood loss, intraoperative transfusion volume, postoperative hospital stay, and PSM rates (all P>0.05). This study also innovatively introduced and compared metrics such as postoperative 24-hour drainage volume, total postoperative drainage volume, duration of postoperative drain indwelling, and duration of postoperative catheter indwelling, further confirming no significant differences in perioperative outcomes between the groups.

We speculate that the lack of significant differences in perioperative outcomes between the two groups may be attributed to the following reasons: first, although they differ in biological behaviors such as tumor invasiveness, perioperative indicators primarily reflect surgical trauma and the patient’s immediate recovery capacity, which are less directly influenced by the inherent malignancy degree of the tumor itself (16). Second, the technical advantages of robotic surgery might partially offset potential differences. Literature confirms that the robotic surgical system provides a high-definition, magnified field of view and more flexible, precise operating instruments, significantly enhancing the precision and stability of surgical maneuvers (17,18), thereby effectively reducing the impact of tumor morphology on perioperative indicators. Even when facing potentially locally complex situations in OmPCa, RARP can effectively control surgical trauma, resulting in comparable metrics to those of LPCa surgery (19). The study by Beyatl et al. (14) showed that OmPCa did not increase the mean hospital stay (4.85 vs. 5.32 days, P=0.25) or perioperative complication rates (P=0.83). Another study (20) reported that the median operative time, intraoperative blood loss, hospital stay, and complication rate for OmPCa patients undergoing RARP were 147 min, 300 mL, 5 days, and 15.6%, respectively, all similar to the perioperative data for RP treating LPCa reported in previous meta-analyses (21). The perioperative outcomes of our study are largely consistent with these findings.

Although the minimal complication rate observed in the oligometastatic cohort is clinically reassuring and supports our preliminary conclusion regarding procedural safety, a key methodological consideration must be noted in the interpretation of this finding. A post hoc power analysis (using PASS software, version 15.0) indicated that, with the present sample size (n=100 per group), the study possessed only approximately 25% power to detect the observed absolute difference of 2% in complication rates (two-sided α=0.05). Therefore, while the numerically low and statistically non-significant difference in complications is encouraging, the study remains underpowered to definitively rule out a clinically meaningful increase in risk. Consequently, the non-significant P value should be interpreted with caution and cannot be construed as evidence of equivalence between the two groups.

Postoperative urinary continence is the most critical factor evaluating patients’ quality of life and satisfaction after surgery (22); therefore, whether OmPCa affects postoperative urinary continence has attracted significant attention. Previous studies have indicated (23,24) that compared to surgery alone, postoperative adjuvant radiotherapy might delay urinary continence recovery and prolong the duration of UI symptoms. Consequently, this study excluded the potential influence of postoperative radiotherapy on urinary continence function in its analysis. In this study, we report no significant differences between the OmPCa and LPCa groups in the EPIC UI domain scores, nor were there statistically significant differences in postoperative UI recovery rates. Similarly, in a study focusing on RARP for OmPCa, Chen et al. (25) also observed no significant differences in UI recovery rates at 3, 6, and 12 months postoperatively compared to the LPCa group (all P>0.05). Previous literature reported that UI recovery rates at 3 and 12 months after non-nerve-sparing RP for LPCa patients were 62.2–72.6% (26,27) and 76.9–91.0% (28-30), respectively, which are close to the UI recovery rates observed in the OmPCa group of this study. These findings preliminarily suggest that OmPCa has a limited impact on patients’ postoperative urinary continence function.

Regarding erectile function, EPIC sexual domain scores indicated poorer postoperative sexual function in the OmPCa group, and the incidence of ED at 1 year postoperatively was significantly higher than in the LPCa group. Our findings demonstrate that, compared to LPCa, OmPCa patients undergoing RARP experience a more clinically significant decline in postoperative sexual function. Postoperative erectile function in PCa patients is primarily influenced by the extent of damage to anatomical structures like the NVB and other postoperative treatments (31). Although both groups underwent non-nerve-sparing techniques and showed no significant differences in the proportion receiving postoperative radiotherapy (21.0% vs. 17.0%, P=0.47) or using PDE5is (79.0% vs. 72.0%, P=0.25), the proportion receiving ADT postoperatively was significantly higher in the OmPCa group due to its higher tumor burden (100.0% vs. 23.0%, P<0.001). This likely contributed to the poorer erectile function in this group, rather than being a direct consequence of the surgery itself. Furthermore, studies indicate that the incidence of ED in the population aged ≥60 years can be as high as 60% (32-34), and sexual activity needs decrease significantly in older populations (35); the median age of OmPCa patients in this study was 68 (IQR, 64, 72) years, classifying them as an older population. Therefore, we believe that the impact of RARP combined with endocrine therapy for OmPCa on postoperative erectile function is within an acceptable range.

The following limitations of this study should be noted: first, this was a retrospective study design, carrying inherent risks of potential bias. Second, due to stringent imaging-based inclusion criteria, the sample size is limited, which may restrict the interpretation of some outcomes. Additionally, a small number of patients in the LPCa group underwent only preoperative imaging evaluation without PLND, which might have led to disease stage underestimation. Moreover, the study period was relatively long (13 years), during which evolution in PET/CT tracers, surgical techniques and perioperative management strategies might have influenced the outcome measures to some extent. Notably, Kim et al. (36) suggested that a higher preoperative serum testosterone level is one factor affecting postoperative ED recovery; future studies should include this metric to exclude its potential influence.

Conclusions

In conclusion, this study demonstrates that compared to LPCa patients, RARP does not increase the risk of perioperative adverse outcomes or postoperative functional decline in patients with OmPCa. This finding provides evidence for expanding the surgical indications for RARP in the treatment of OmPCa. Future prospective studies are warranted to provide higher-level evidence.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-aw-527/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-aw-527/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-aw-527/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-aw-527/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The protocol was approved by the Ethics Committee of Chinese PLA General Hospital (No. S2025-406-01), The First Affiliated Hospital of Nanchang University (No. IIT-2024-657) and The First Affiliated Hospital of Soochow University (No. 2026-198). All eligible patients provided written informed consent. All participating hospitals were informed and agreed on the study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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