Limited data are available on the role of robot-assisted radical prostatectomy (RARP) in patients with locally advanced prostate cancer (PCa).
To describe our surgical technique of extrafascial RARP and extended pelvic lymph node dissection (ePLND) in locally advanced PCa.
Design, setting, and participants
Ninety-four patients with clinical stage ≥T3 undergoing RARP with ePLND at three European centers between 2011 and 2015 were retrospectively evaluated.
Surgery was performed using the DaVinci Si system. The anatomically defined ePLND included nodes overlying the external iliac axis, those in the obturator fossa, and around the internal iliac artery up to the ureter. RARP was performed using an extrafascial approach where the Denonvillers’ fascia was dissected free and left on the posterior surface of the seminal vesicles.
Perioperative outcomes consisted of operative time, blood loss, length of hospital stay, and complications occurred within 30 d after surgery. Biochemical recurrence (BCR) was defined as two consecutive prostate-specific antigen values ≥0.2 ng/ml. Kaplan-Meier analyses assessed time to BCR and clinical recurrence. Multivariable Cox regression analyses assessed predictors of BCR.
Results and limitations
Median operative time, blood loss, and length of hospital stay were 230 min, 200 ml, and 6 d. Overall, 12 (12.7%) patients experienced complications and five (5.3%), four (4.3%), and three (3.2%) patients had Clavien I, II, and III/IV complications. Overall, 72 (76.6%), 35 (37.2%), and 30 (32.3%) patients had pT3/4, pN1, and positive margins. The median number of nodes removed was 16. Overall, 19 (20.2%) and 21 (22.3%) patients received adjuvant radiotherapy and hormonal therapy. The median follow-up was 23.5 mo. At 3-yr follow-up, the BCR- and clinical recurrence-free survival rates were 63.3% and 95.8%. Pathologic stage, Gleason score, and positive margins represented predictors of BCR (all p ≤ 0.03). Our study is limited by its retrospective nature and by the follow-up duration.
RARP represents a well-standardized, safe, and oncological effective option in patients with locally advanced PCa. Pathologic stage, Gleason score, and positive margins should be considered to select patients for multimodal approaches.
Robot-assisted surgery represents a well-standardized, safe, and oncological effective option in men with locally advanced prostate cancer. Two out of three patients treated with this approach are free from recurrence at 3-yr follow-up. Pathologic stage, Gleason score, and positive surgical margins represent predictors of BCR and should be considered to select patients for multimodal approaches.
Keywords: Prostate cancer, Radical prostatectomy, Extended pelvic lymph node dissection, Locally advanced, Robot assisted.
Although the introduction and diffusion of prostate-specific antigen (PSA)-based screening dramatically increased the proportion of patients diagnosed with low-risk prostate cancer (PCa) , up to 10% of contemporary individuals still present with locally advanced disease . These men should be deemed at very high risk of recurrence according to clinical guidelines . For this reason, they were historically considered as ideal candidates for the administration of systemic therapies upfront , , and . However, recent studies demonstrated that surgery alone or in combination with additional treatments such as radiotherapy and androgen deprivation therapy might represent oncologically safe options even in this setting, where the 5-yr cancer-specific mortality-free survival rates of patients with high-risk PCa treated with laparoscopic or open radical prostatectomy (RP) exceeded 90% , , , and .
Robot-assisted radical RP (RARP) currently represents the most commonly performed surgical procedure in men with localized PCa . Although concerns related to the increased risk of complications and poor oncologic control related to the lack of haptic feedback initially limited the diffusion of this approach to patients with high-risk disease, recent investigations demonstrated that RARP represents a safe and effective procedure even in this setting , , , and . However, none of the currently available reports focused specifically on men with locally advanced disease. Under this light, we sought to describe our surgical technique of extrafascial RARP and extended pelvic lymph node dissection (ePLND) in patients with a clinical stage ≥T3 treated at three high-volume European centers. Moreover, we aimed at reporting perioperative and oncologic outcomes of these patients.
2. Materials and methods
2.1. Patient population
After Ethical Committee approval, 94 patients with locally advanced PCa as defined by clinical stage T3 or higher at digital rectal examination (ie, tumor extended through the prostatic capsule with or without involvement of the seminal vesicles or adjacent structures) and/or preoperative multiparametric magnetic resonance imaging were retrospectively identified. Patients were treated with RARP and ePLND at three high-volume European centers between January 2011 and June 2015.
2.2. Surgical technique
All procedures were performed through a six-port transperitoneal approach using the four-arm Da Vinci Si (Intuitive Surgical, Sunnyvale, CA, USA) Robotic Surgical System. The following robotic instruments were used: monopolar scissors, fenestrated bipolar forceps or Maryland bipolar forceps, prograsp forceps, and large needle driver. After incision of the peritoneum, release of the bladder laterally to the endopelvic fascia, and localization of the ureter, the dissection of the lymphatic tissue was performed adopting the split and roll technique. The external iliac artery was localized behind the peritoneum. The peritoneal incision was prolonged following the external iliac artery up to the vas deferens, which was exposed and then cut. The fibrofatty tissue along the external iliac vein was dissected, the lateral limit being the genitofemoralis nerve and the distal limit being the deep circumflex vein. Proximally, ePLND was performed up to and included the crossing between the ureter and common iliac vessels. Once the external iliac vessels were freed, the obturator nerve was approached. The dissection was performed from lateral to medial up to the umbilical artery and the bladder wall that represented the medial limit of the ePLND. Lymph nodes along as well as medially and laterally to the internal iliac vessels were also removed (Fig. 1). The obturator fossa was also accessed lateral to the external iliac artery and the lymphatic tissue freed from the pelvic wall. Smaller vessels were coagulated and cut and dissection was continued until the deep obturator fossa was reached. All fibrofatty tissue within the obturator fossa was removed. The Marcille's triangular lumbosacral fossa was dissected free (Fig. 2). This area was delimited laterally by the medial border of the psoas, medially by the body of the fifth lumbar vertebra, and inferiorly by the border of the sacral wing .
The external and internal iliac arteries, the ureter, and the genitofemoralis nerve were localized before performing an extended pelvic lymph node dissection.
Access to the Marcille's triangle during robot-assisted extended pelvic lymph node dissection. The psoas muscle, external iliac vessels, and obturator nerve are clearly identifiable.
Bladder detachment, endopelvic fascia incision, bladder neck incision, ligation of the dorsal venous complex, apical dissection, posterior reconstruction, and urethro-vesical anastomosis were then performed according to previously described techniques , , and . During isolation and dissection of seminal vesicles the Denonvillers’ fascia was incised. The perirectal fatty tissue was then entered and dissection was performed following the plan between the rectum and the posterior aspect of the Denonvillers’ fascia. As a result, the Denonvillers’ fascia was completely dissected free and left on the posterior surface of the seminal vesicles, thus ensuring oncological safety of the procedure (Fig. 3). The extrafascial dissection was subsequently carried out laterally to the levator ani fascia. During this approach the neurovascular bundles were clipped and transected below the Denonvillers’ fascia. This surgical technique resulted into a large amount of tissue surrounding the pathologic specimen.
The Denonvillers’ fascia was completely dissected free and left on the posterior surface of the seminal vesicle during the extrafascial dissection.
2.3. Covariates and outcomes
All patients included in the study had complete preoperative and pathologic data including clinical stage, biopsy Gleason score, PSA at diagnosis, percentage of positive cores, pathologic stage, pathologic Gleason score, number of nodes removed, and of positive nodes, and positive margins. Perioperative outcomes consisted of operative time, blood loss, length of hospital stay, and 30-d postoperative complications (categorized according to the Clavien-Dindo classification). Adjuvant radiotherapy and androgen deprivation therapy were administered in patients with aggressive pathologic characteristics (ie, pathologic Gleason score 8–10, lymph node invasion, positive margins, and nonorgan confined disease) according to the clinical judgment of the treating physician and after discussion with the patient regarding the benefits and possible side effects. Patients underwent follow-up visits every 3 mo during the 1st yr after surgery and every 6 mo thereafter. Urinary continence was defined as the use of no pads over the 24-h period. Biochemical recurrence (BCR) was defined as two consecutive increases in PSA ≥0.2 ng/ml. Clinical recurrence (CR) was defined as positive imaging during follow-up after the onset of BCR.
2.4. Statistical analysis
Medians and interquartile ranges were reported for non-normally distributed continuous variables. Frequencies and proportions were reported for categorical variables. Kaplan-Meier analyses assessed time to BCR and CR. These analyses were repeated in patients who did not receive neoadjuvant androgen deprivation therapy (n = 85) and in a cohort of patients who did not receive any adjuvant treatment (n = 70). Multivariable Cox regression analyses assessed predictors of BCR in the entire cohort. Covariates consisted of pathologic stage, pathologic Gleason score, lymph node invasion, positive surgical margins, and the administration of adjuvant therapies. All statistical analyses were performed using the R statistical package v.3.0.2 (R Project for Statistical Computing, Vienna, Austria). All tests were two sided, with a significance level set at p < 0.05.
3.1. Baseline and pathologic characteristics
Table 1 depicts demographic and tumor characteristics of the study cohort. All patients included in the study had clinical stage T3 or higher. The median lymph node yield was 16. Overall, 22 (23.4%), 31 (33.0%), 40 (42.6%), one (1.1%), and 35 (37.2%) patients had pathologic stage pT2, pT3a, pT3b, pT4, and pN1, respectively. The median number of positive nodes was three. Overall, 32.3% patients had positive surgical margins. Overall, eight (8.5%), 47 (50.0%), and 39 (41.5%) patients had pathologic Gleason score 7, 8, and 9–10, respectively.
Clinical and pathologic characteristics of prostate cancer patients with locally advanced disease (clinical stage ≥ cT3) treated with robot-assisted radical prostatectomy
|N = 94|
|Age at surgery|
|Median (IQR)||64.3 (57.1–68.9)|
|Median (IQR)||25.0 (23.9–27.4)|
|CCI index (%)|
|PSA at diagnosis|
|Median (IQR)||9.7 (5.1–17.5)|
|Biopsy Gleason score (%)|
|Number of biopsy cores taken|
|Median (IQR)||12 (8–16)|
|Number of biopsy cores positive|
|Median (IQR)||6 (4–9)|
|Percentage of positive cores (%)||50.0 (40.0–72.3)|
|Pathologic stage (%)|
|Pathologic Gleason (%)|
|Number of nodes removed|
|Median (IQR)||16 (8–24)|
|Lymph nodes invasion (%)||35 (37.2)|
|Number of positive nodes|
|Median (IQR)||3 (2–6)|
|Positive surgical margins (%)||30 (32.3)|
|Neoadjuvant HT||10 (10.6)|
|Adjuvant RT (%)||19 (20.2)|
|Adjuvant HT (%)||21 (22.3)|
|Salvage RT (%)||7 (7.4)|
|Salvage HT (%)||8 (8.5)|
BMI = body mass index; IQR = interquartile range; HT = hormonal therapy; RT = radiotherapy.
3.2. Perioperative outcomes
Table 2 lists perioperative parameters. Median operative time was 230 min. Median blood loss was 200 ml and four (4.3%) patients were transfused after surgery for postoperative anemia. Overall, 12 (12.7%) patients experienced postoperative complications. When postoperative complications were stratified according to the Clavien-Dindo system, five (5.3%), four (4.3%), two (2.1%), and one (1.1%) patients had Grade I, II, III, and IV complications, respectively. When considering PLND-related complications, three patients had pelvic lymphoceles and one had prolonged lymphorrhoea. In one case the pelvic lymphocele was managed with percutaneous drainage. No perioperative mortality was observed. The median length of hospital stay was 6 d. Overall, 63 patients had complete data on urinary continence after surgery. The 1-yr urinary continence recovery rate was 64.0%.
Perioperative outcomes of prostate cancer patients with locally advanced disease (clinical stage ≥ cT3) treated with robot-assisted radical prostatectomy
|N = 94|
|Operative time (min)|
|Median (IQR)||230 (180–266)|
|Blood loss (ml)|
|Median (IQR)||200 (150–350)|
|Postoperative complications (%)||12 (12.7)|
|Clavien-Dindo classification (%)|
|Anastomotic leak||1 (1.1)|
|Postoperative anemia||4 (4.3)|
|Lower extremity compression injury||1 (1.1)|
|Pelvic hematoma||1 (1.1)|
|Acute myocardial infarction||1 (1.1)|
|Postoperative transfusion (%)||4 (4.3)|
|Length of stay (d)|
|Median (IQR)||6 (3–6)|
IQR = interquartile range.
3.3. Survival analyses
Median (interquartile range) follow-up after surgery was 23.5 (18.7–27.3) mo. Overall, 19 (20.2%) and 21 (22.3%) patients received adjuvant radiotherapy and hormonal therapy, respectively. Overall, 21 and three patients experienced BCR and CR, respectively. No patients experienced cancer-specific mortality. At 3-yr follow-up, the BCR-free and CR-free survival rates were 63.3% and 95.8%, respectively (Fig. 4). When considering patients who did not receive neoadjuvant hormonal treatments, the 3-yr BCR- and CR-free survival rates were 66.3% and 95.4%, respectively. When considering patients who did not receive any adjuvant treatment, the 3-yr BCR- and CR-free survival rates were 67.0% and 96.2%, respectively.
Kaplan-Meier analyses assessing time to (a) biochemical recurrence (BCR) and (b) clinical recurrence (CR) in patients with locally advanced prostate cancer treated with robot-assisted radical prostatectomy.
CE = cumulative events; NR = number at risk.
At multivariable Cox regression analyses, pathologic stage, pathologic Gleason score, and the presence of positive surgical margins represented independent predictors of BCR (Table 3; all p ≤ 0.03) after adjusting for the administration of adjuvant therapies and lymph node invasion.
Multivariable analyses assessing predictors of biochemical recurrence in prostate cancer patients with locally advanced disease (clinical stage ≥ cT3) treated with robot-assisted radical prostatectomy
|HR (95% CI)||p value|
|Lymph nodes invasion||1.60 (0.52–4.93)||0.4|
|Positive surgical margins||6.28 (1.82–21.4)||0.01|
|Adjuvant treatments||0.67 (0.21–2.15)||0.5|
CI = confidence interval; HR = hazard ratio; Ref. = reference.
Nowadays RARP represents the most widely adopted surgical treatment among patients with localized PCa, where more than 85% of RPs are currently performed using this approach in the US alone  and . Due to the learning curve phenomenon, as well as lack of haptic feedback and difficulties in performing ePLND, the use of this minimally invasive technique was initially restricted to men with more favorable disease characteristics , , , and . Only in recent years RARP has been proved as a safe and oncologically effective procedure even in the high-risk scenario , , and . However, none of the currently available series specifically focused on individuals with locally advanced disease. Our hypothesis is that the advantages of RARP in the hands of experienced surgeons in terms of reduced blood loss, tissue magnification and recognition, and tridimensional vision would result into optimal cancer control even in this setting. Therefore, we aimed at describing our surgical technique of extrafascial dissection and ePLND in men with locally advanced disease as defined by preoperative magnetic resonance imaging or digital rectal examination. Moreover, we sought to report perioperative and oncologic outcomes of patients with cT3 or higher PCa treated with RARP and ePLND in three high-volume European institutions and to identify predictors of recurrence.
Our results are several fold. Firstly, we observed excellent perioperative outcomes, where approximately one out of 10 patients experienced postoperative complications within 30 d from surgery and only two (2.2%) individuals had Grade III or IV complications according to the Clavien-Dindo classification. In addition, more than 60% of patients included in our cohort experienced continence recovery within 12 mo after surgery. Although this represents the first investigation focusing exclusively on individuals with clinical stage T3 or higher, previous studies reported acceptable perioperative outcomes in high-risk patients undergoing robot-assisted surgery  and . For example, a large population-based investigation including men older than 65 yr treated in the US demonstrated that less than 30% of them experienced postoperative complications . Moreover, comparative studies reported similar rates of complications among high-risk men treated with minimally invasive and open surgery  and . However, the main advantage of the minimally invasive approach compared with the open technique in terms of perioperative outcomes would reside into a lower risk of bleeding and postoperative transfusions  and . Under this light, it is worth mentioning that the median blood loss of patients included in our cohort was only 200 ml and that less than 5% of them necessitated a blood transfusion in the postoperative period. Finally, up to 64% of patients were continent at 1-yr follow-up. The relatively low continence recovery rate observed in our analysis might be related to the stringent definition applied, as well as to the inclusion of men with locally advanced disease treated with non-nerve sparing approaches, where the degree of preservation of neurovascular bundles might be correlated with recovery of early continence after RARP  and . Taken together, these observations support the safety of RARP in men with locally advanced disease.
When considering pathologic results, the robotic approach was able to achieve an adequate nodal staging in our series, where a median of 16 nodes were removed with a lymph node invasion rate of approximately 40%. All patients received an anatomically defined ePLND that included the lymph nodes overlying the external iliac axis, those in the obturator fossa and around the internal iliac artery up to the crossing between the ureter and the iliac vessels, according to clinical guidelines . This template would allow to correctly stage up to 94% of the patients with node-positive disease and to remove all the metastatic nodes in approximately 75% of the cases . Moreover, the Marcille's triangular lumbosacral fossa was dissected free, where the inclusion of this area would increase the number of nodes removed in patients undergoing robotic surgery . Although historical studies questioned the ability of robot-assisted approaches to remove an adequate number of nodes in men with aggressive disease , our observations, together with other recent investigations, support the feasibility of an anatomically defined ePLND performed using this minimally invasive technique  and . In this context, it should be noted that individual surgeon experience and commitment rather than the surgical approach itself would have a significant impact on the extension of PLND and on the number of nodes removed .
Another proxy of surgical quality is represented by the rate of positive surgical margins. Approximately 30% of men undergoing RARP with extrafascial dissection included in our cohort experienced positive margins at final pathology. Although these results are in line with other studies that focused on patients with high-risk disease according to the D’Amico classification , , , , and , we should highlight that our is the first investigation focusing exclusively on men with locally advanced disease at diagnosis treated with robotic surgery. When evaluating individuals with cT3 disease treated with open radical prostatectomy, Mitchell et al  reported that the positive margin rate exceeded 50%. The lower rates observed in our study might be related to the better visualization of the prostate and apex secondary to tissue magnification, reduced intraoperative bleeding, and tridimensional vision associated with the minimally invasive approach. Under this light, comparative studies demonstrated that these advantages would result into a lower risk of positive margins associated with RARP particularly in the high-risk setting  and . Our investigation was also able to provide data on the risk of recurrence. In particular, at 3-yr follow-up more than two out of three patients were free from BCR. In addition, the CR-free survival rates at this time point exceeded 95%. This held true even after excluding patients who received neoadjuvant or adjuvant treatments. Taken together, these results support the oncological safety of the proposed surgical technique in terms of the risk of recurrence. Nonetheless, it should be noted that the relatively short follow-up of our cohort in part limits its generalizability. Although previous studies reported the long-term outcomes of open or laparoscopic surgery in men with locally advanced disease (Table 4), our investigation represents the first study specifically focusing on patients treated with the robotic approach , , , , and . Further studies are needed to confirm the effectiveness of RARP at long-term follow-up in this clinical scenario. Finally, our analyses identified pathologic stage, positive margins, and pathologic Gleason score as independent predictors of recurrence. However, lymph node invasion was not associated with the risk of BCR. This might be related to the relatively high rate of men with pN1 (approximately 40%) observed in our cohort of locally advanced PCa patients, as well as to the relatively short follow-up. Adverse pathologic characteristics such as positive margins, pT3b/4 disease, and pathologic Gleason score 8–10 should be considered for the identification of patients who might benefit from a multimodal approach after surgery even in the setting of locally advanced PCa .
Results of series evaluating oncologic outcomes of radical prostatectomy in the management of patients with locally advanced prostate cancer
|First authors and yr||Definition||Technique||Number of patients||Neoadjuvant therapies (%)||Median follow-up (mo)||Number of nodes removed||Positive margins (%)||Adjuvant therapies (%)||Oncologic outcomes|
|Van Poppel et al 2000||Clinical stage T3||Open||158||30a||NA||60||30.3||3-yr BCR-free survival: 40%|
|Carver et al 2006||Clinical stage T3||Open||176||36||76.8a||NA||27||10-yr BCR-free survival: 44%|
10-yr CR-free survival: 76%
|Xylinas et al 2009||Clinical stage T3||Open retropubic (n = 77) or laparoscopic (n = 23)||100||69||NA||61||31||5-yr BCR-free survival: 45%|
5-yr CSM-free survival: 90%
|Mitchell et al 2012||Clinical stage T3||Open||843||24||171||NA||56||ADT: 40.8|
|20-yr local recurrence-free survival: 76%|
20-yr systemic progression-free survival: 72%
20-yr CSM-free survival: 81%
|Gozen et al 2015||Clinical stage T3||Laparoscopic||492||NA||104||13.9||38.2||ADT: 49.2|
|10-yr CSM-free survival: 97.4%|
ADT = androgen deprivation therapy; BCR = biochemical recurrence; CR = clinical recurrence; CSM = cancer-specific mortality; NA = not available; RT = radiotherapy.
Despite several strengths, our study is not devoid of limitations. Firstly, it is limited by its retrospective nature. Secondly, a longer follow-up might be needed to comprehensively assess oncologic outcomes of RARP and ePLND in men with locally advanced PCa. Nonetheless, our analyses were able to demonstrate excellent 3-yr recurrence-free survival rates. Thirdly, the inclusion of patients treated at three different European centers might have introduced elements of heterogeneity with regards to patient selection, surgical technique, as well as pathologic assessment, where a central review was not performed. Nonetheless, our study takes advantages from the high-volume nature of the institutions included and from the availability of dedicated experienced uropathologists. Moreover, the inclusion of patients who received neoadjuvant androgen deprivation therapy might affect pathologic results. However, this treatment modality was administered in less than 10% of patients included in our cohort. Finally, it should be noted that these results were obtained in the setting of referral centers and high-volume surgeons. Given the association between hospital volume, surgical experience, and perioperative and oncologic outcomes after surgery in PCa, this might limit the generalizability of our findings to other contexts.
RARP represents a well-standardized, safe, and effective option in patients with locally advanced PCa, where excellent perioperative results and oncologic outcomes are observed at intermediate-term follow-up. In particular, two out of three patients are free from recurrence at 3 yr after surgery. Pathologic stage, Gleason score, and positive margins represent predictors of recurrence and should be considered to select patients for multimodal approaches.
Author contributions: Giorgio Gandaglia had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Mottrie, Gandaglia, Briganti, Montorsi, Novara, Rocco, Suardi.
Acquisition of data: De Groote, De Lorenzis, Fossati.
Analysis and interpretation of data: Gandaglia, Mottrie, Briganti, Montorsi.
Drafting of the manuscript: Gandaglia, Mottrie, Novara, Dovey, Rocco, Montorsi, Briganti.
Critical revision of the manuscript for important intellectual content: Mottrie, Montorsi, Novara, Suardi, Briganti.
Statistical analysis: Gandaglia.
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Mottrie, Montorsi, Briganti, Novara.
Financial disclosures: Giorgio Gandaglia certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: None.
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a Division of Oncology/Unit of Urology, Urological Research Institute, IRCCS Ospedale San Raffaele, Milan, Italy
b Department of Urology, Vita-Salute San Raffaele University, Milan, Italy
c OLV Vattikuti Robotic Surgery Institute, Melle, Belgium
d Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milano, Italy
e Department of Urology, Onze-Lieve-Vrouw Hospital, Aalst, Belgium
Corresponding author. Division of Oncology/Unit of Urology, Urological Research Institute, IRCCS Ospedale San Raffaele, Via Olgettina 58, Milan 20132, Italy. Tel. +39 0226437286; Fax: +39 0226437286.
© 2016 European Association of Urology, Published by Elsevier B.V.