Prostate International xxx (xxxx) xxx

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Prostate International
journal homepage: https://www.journals.elsevier.com/prostate-international

Research Article

Comparing open and robotic salvage radical prostatectomy after

radiotherapy: predictors and outcomes
Pablo F. Martinez, Agustin Romeo*, Ignacio Tobia, Mariana Isola, Carlos R. Giudice,
Wenceslao A. Villamil
Urology Department, Hospital Italiano de Buenos Aires, Argentina

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: In the present study, we aim to provide more evidence about benefits of salvage radical
Received 30 May 2020 prostatectomy (SRP). Our main objective is to assess prostatic-specific antigen control and postoperative
Received in revised form urinary incontinence in open and robotic approaches as primary outcomes.
26 June 2020
Materials and methods: After the Institutional Review Board approval (IRB00010193), we retrospec-
Accepted 19 July 2020
tively analyzed 76 consecutive patients who underwent open or robot-assisted SRP for locally relapsed
Available online xxx
prostate cancer between 2004 and 2019 at the Urology Department of Hospital Italiano de Buenos Aires,
Argentina. Data were collected from our electronic medical record and prospective database.
Keywords:
Urinary incontinence
Postoperative variables, such as urinary incontinence, erectile function preservation, and vesicourethral
Prostate cancer anastomosis stricture development, were analyzed.
Radiotherapy Results: Before SRP, 59 patients (76.6%) were treated with 3D external beam radiotherapy, 11 (14.3%)
Robotic surgery with brachytherapy, and 6 (7.8%) with intensity-modulated radiotherapy. Fifty patients underwent open
Salvage radical prostatectomy SRP, and 26, robot-assisted SRP. Comparing surgical approaches, the global incontinence rate was 34.2%
versus 9.1% in open versus robot-assisted approach, respectively (p: 0.01).
Vesicourethral anastomosis stricture occurred in six patients (8.7%), all in the open approach group (p:
0.07). Five patients of 69 (7.2%) preserved erectile function with/without use of phosphodiesterase 5
inhibitors. Two patients in the open approach group needed blood transfusion. Estimated 2-year
biochemical recurrenceefree survival rate in the open approach group and robot-assisted group was
67% (95% confidence interval: 53.7e80.3) and 60.9% (95% confidence interval: 40.5e81.3), respectively,
with no statistical difference (log-rank test p: 0.873).
Conclusions: Robot-assisted SRP is a reliable procedure to treat local recurrences after external beam
radiotherapy or brachytherapy, reducing the risk of anastomotic strictures and blood loss and improving
continence outcomes.
© 2020 Asian Pacific Prostate Society. Publishing services by Elsevier B.V. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction interval from BCR to development of distant metastases is

approximately 3 years4; thus, these patients have an important
Prostate cancer (PCa) represents the most commonly diagnosed opportunity for a definitive curative treatment. However, curative
noncutaneous cancer in men worldwide1. External beam radio- options are rarely contemplated as 90% of men with recurrence are
therapy (EBRT) or brachytherapy (BT) are well-known treatment treated with palliative systemic androgen deprivation therapy
modalities for newly diagnosed patients with clinically localized (ADT), experiencing related adverse effects and losing cancer con-
PCa. Nearly 30% to 60% of the patients will undergo biochemical trol opportunity5.
recurrence (BCR) within the first 5e10 years after treatment2,3. In Even more, most of them develop castration resistance at
the absence of any salvage therapy after proven relapse, the median 5 years on average6,7.Salvage radical prostatectomy (SRP) is a
technically demanding and challenging surgery. Historical open
SRP series were associated with a higher morbidity rate; rectal
injury could be observed in 19% of patients, urinary extravasations
n 4190
* Corresponding author. Hospital Italiano de Buenos Aires, Juan D. Pero
(C1181ACH), Buenos Aires, Argentina in 5%, bladder neck stricture in 40%, and persistent post-
E-mail address: [email protected] (A. Romeo). prostatectomy urinary incontinence (UI) in 5-76.9% 8,9. Oncologic

https://doi.org/10.1016/j.prnil.2020.07.003
p2287-8882 e2287-903X/© 2020 Asian Pacific Prostate Society. Publishing services by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article as: Martinez PF et al., Comparing open and robotic salvage radical prostatectomy after radiotherapy: predictors and
outcomes, Prostate International, https://doi.org/10.1016/j.prnil.2020.07.003
2 Prostate International xxx (xxxx) xxx

results were also discouraging, with positive surgical margin (PSM) 2.3. Statistical analysis
rates ranging 70% and BCR rates at 10 years of 82%5.
Despite the widespread use of robotic surgery, at present only a Continuous variables were presented as median and inter-
small number of robotic SRP series have been published, showing quartile range (IQR) and for their comparison ManneWhitney was
significant improvements in functional outcomes and decreases in used. Categorical variables were summarized as counts (frequency
complications. A recent large multicenter study showed a higher percentages), and they were compared with the Chi-square test or
degree of continence preservation, reaching 63.9%, and a reduced the Fisher's exact test when appropriate.
anastomotic stricture rate of 7.6%, all of them in the robotic surgery Univariate analysis for 1-year UI was performed by multinomial
group5. logistic regression because all patients were evaluated at this time.
However, the European Association of Urology guidelines advise Regression results were expressed as the odds ratio (OR) with 95%
that strong recommendations regarding SRP cannot be made, as the confidence interval (CI 95%).
available evidence for this treatment option is scarce and of very Survival curves were presented as KaplaneMeier curves, and
low quality10. the log-rank test was used for comparison between groups. All of
In the present study, we aim to provide more evidence about the analyses were considered significant at a two-tailed P-value of
benefits of SRP. 0.05.
Our main objective is to assess prostatic-specific antigen (PSA) All statistical tests were performed using statistical software
control and postoperative UI in open and robotic approaches as SPSS 23.0 TM for Microsoft (SPSS Inc; IBM, Chicago, IL) and STATA
primary outcomes. 8.0 TM version for Microsoft (Statacorp LP, College Station,TX).

2. Materials and Methods

After Institutional Review Board approval (IRB00010193), we

retrospectively analyzed 76 consecutive patients who underwent 3. Results
open or robot-assisted SRP for locally relapsed PCa between August
2004 and March 2019 at the Urology Department of Hospital Ital- A total of 76 patients were included in the study, with a median
iano de Buenos Aires, Argentina. Our center has a mean caseload of age at time of salvage prostatectomy of 64.5 years (IQR: 60-68).
200 radical prostatectomies per year, and SRP was performed only Before SRP, 59 patients (77.6%) received 3D EBRT, 11 (14.5%) BT, and
by three experienced surgeons beyond their learning curve. 6 (7.9%) intensity-modulated radiotherapy. Gleason score
7 was
Data were collected from our electronic medical record and the observed in 39 patients (51.3%) on preradiotherapy biopsy.
prospective database. All patients underwent confirmatory pros- Regarding the Gleason 7 group, 27 (84.3%) patients received a
tate biopsy before SRP. combination of ADT plus RT and five patients (15.6%) RT alone. In
Postoperative variables, such as UI, erectile function preserva- the Gleason 8 group, one patient received RT alone and six patients
tion, and vesicourethral anastomosis stricture development, were (85.7%) ADT plus RT.
analyzed. Clinicopathological features of patients who underwent SRP are
summarized in Table 1.
A large proportion of patients had high-risk PCa in pathological
2.1. Surgical approach specimens after SRP. Gleason score 8 or greater (International So-
ciety of Urologic Pathologists "ISUP" grade 4/5) was observed in
Open SRP was performed using the standard retropubic tech- 68.4% and locally advanced disease (pT3a/pT3b) in 60%. PSMs were
nique. Robot-assisted SRP was performed using the transperitoneal observed in 28.9% of the patients, overall. Extended lymph node
approach with the da Vinci Si HD Surgical System (Intuitive Sur- dissection was attempted in all cases and achieved in 72 patients
gical, Sunnyvale, CA, USA). Extended lymph-node dissection was (94.7%). In the remaining four patients, lymph node dissection
attempted in all cases. Preservation of the neurovascular bundles could not be performed because of extreme fibrosis in the surgical
was attempted only with patients that were preoperatively potent, field. Involved lymph nodes were found in five patients (6.6%).
when it was oncologically feasible and in accordance with intra- Postoperative complications ClavieneDindo grade III-V were
operative findings. For neurovascular bundle preservation, dissec- observed in seven patients (9.2%). Four patients developed uro-
tion was always performed in an interfascial fashion. sepsis, and two patients developed atrial fibrillation with rapid
ventricular response; all of them resolved with medical treatment.
2.2. Definitions One patient developed hematuria and was treated with cystoscopy
for clot evacuation.
BCR after radiotherapy (RT) is defined by the American Society With a median bladder catheterization time of 15 days, urinary
for Therapeutic Radiation and Oncology as a rise in serum PSA by leakeage was infrequent and observed only in one patient in the
2 ng/ml from a nadir PSA. BCR after SRP was defined as PSA
0.2 ng/ robotic group. Open reanastomosis was performed and patient
ml, followed by a subsequent confirmatory PSA value
0.2 ng/ml11. recovered uneventfully.
The definition of continence was based on the response to “How Rectal injury was observed in one patient (3.8%) in the robotic
many pads per day did you usually use to control urinary leakage?“. group, p: 0.16. Injury was recognized intraoperatively and repaired
Continence was assessed at 12 months and defined as the use of no primarily with two-layer rectal wall closure as patient had previous
pads. Mild incontinence was defined as the use of 1 pad and bowel preparation. Postoperative was uneventful.
moderate/severe more than 1 pad per day. Although bleeding is more frequent in open surgery, only two
Potency was defined as the ability to achieve and maintain patients (4%) in the open group required blood transfusion. All
erections firm enough for sexual intercourse, with or without the perioperative results are summarized in Table 2.
use of phosphodiesterase 5 (PDE-5) inhibitors. Median follow-up time was 47 months (IQR: 18.5-81); 68 pa-
Intraoperative and postoperative complications within 30 days tients had at least 1 year of follow-up. In this group, UI, erectile
were rigorously recorded and scored as per the ClavieneDindo function, and development of vesicourethral anastomosis stricture
system. were analyzed.

Please cite this article as: Martinez PF et al., Comparing open and robotic salvage radical prostatectomy after radiotherapy: predictors and
outcomes, Prostate International, https://doi.org/10.1016/j.prnil.2020.07.003
 P.F. Martinez et al. / Comparing open and robotic salvage 3

Table 1
Clinicopathological features of patients who underwent SRP.

Variable Total (n:76) Open (n:50) Robot-Assisted (n:26) p-Value

Age pre-RT, median (IQR) 59 (55-62) 60 (56-63) 57 (54-62) 0.073

cTNM pre-SRP (%) 0.659
T1c 43 (56.6) 30 (60) 13 (50)
T2a 9 (11.8) 7 (14) 2 (7.7)
T2b 17 (22.4) 9 (18) 8 (30.8)
T2c 5 (6.6) 3 (6) 2 (7.7)
T3 2 (2.6) 1 (2) 1 (3.8)
Radiotherapy subtype (%) 0.207
Brachytherapy 11 (14.5) 8 (16) 3 (11.5)
3D EBRT 59 (77.6) 40 (80) 19 (73.1)
IMRT 6 (7.9) 2 (4) 4 (15.4)
Gleason sum pre-RT (%) 0.524
6 37 (48.7) 25 (50%) 12 (46.2)
7 32 (42.1) 22 (44) 10 (38.5)
8 7 (9.2) 3 (6) 4 (15.4)
Gleason sum pre-SRP (%) 0.514
6 3 (3.9) 3 (6) 0
7 33 (43.4) 24 (48) 9 (34.6)
8 26 (34.2) 15 (30) 11 (42.3)
9 14 (18.4) 8 (16) 6 (23.1)
ESD pre SRP (%) 17 (22.4) 13 (26) 4 (15.4) 0.292
PSA pre RT, median (IQR) 8 (6.6-11) 8.1 (6.1-10.8) 8 (7.2-11) 0.217
PSA pre SRP, median (IQR) 6.4 (4.1-8.4) 6.1 (4-7.9) 6.5 (4.2-10.3) 0.350
PSA DT median (IQR), months 14.7 (8-25.7) 16.5 (8.2-28.8) 11.6 (7.4-21.8) 0.359
Post RT relapse time, median (IQR), months 42 (24-60) 42 (24.7-72) 39 (24-60) 0.564

EBRT: external beam radiotherapy; ESD: erectile dysfunction; IMRT, intensity-modulated radiotherapy; PSA DT: prostatic-specific antigen doubling time; RT: radiotherapy;
SRP: salvage radical prostatectomy.

3.1. Urinary continence after SRP 3.3. Vesicourethral anastomosis stricture

All patients were continent before SRP. The global UI rate at This event occurred in six patients (8.8%); all of them were in
12 months was 26.4% (18 out of 68 patients). Comparing surgical open approach. p: 0.076.
approaches, the UI rate was 34.2% (16 patients: 10 mild; and 6
patients: moderate/severe grade) versus 9.1% (two patients, both 3.4. Oncological outcomes
mild grade) in the open versus robot-assisted approach, respec-
tively (p: 0.01). Estimated 2-year BCR free survival rate in the open approach
The UI OR in the robot-assisted versus open approach was 0.16 group and robot-assisted group was 67% (CI 95%: 53.7e80.3) and
(CI 95%: 0.03e0.78, p: 0.023). History of BT as primary treatment 60.9% (CI 95%: 40.5e81.3), respectively, with no statistical differ-
also might result as a UI predictor (OR: 4.8, CI 95%: 1.1e20). Overall, ence (log-rank test p: 0.873), Fig. 1.
three patients required an artificial urinary sphincter, with good Regarding the five patients with lymph node involvement (Nþ),
functional outcomes. four of them had a PSA value after SRP lower than 0.20 ng/ml. Three
Regarding severe UI cases, all of these occurred in the open patients with Nþ developed BCR and were treated with ADT. Mean
surgery group (13%), OR: 7.2 (CI 95%: 0.3e134, p ¼ 0.184). For this time to ADT administration in this group was 25 months.
degree of UI, on univariate analysis, history of urethrovesical During follow-up, there were three deaths (two in the open
anastomosis stricture (OR: 7.2, CI 95%: 1e52, p 0.05) and time to versus one in the robot-assisted group) at 12, 39, and 65 months,
bladder catheter removal (OR: 1.3, CI 95%: 1e1.7, p 0.05) may result respectively. The overall cancer-specific survival (CSS) was 95% at
also as predictors. 5 years. We did not evidence any local recurrence after SRP.

4. Discussion

SRP has always been reserved for a minority group of patients

after BCR because of high complications and postoperative
3.2. Erectile function after SRP morbidity rates11. For appropriately selected patients, SRP provides
excellent cancer control without the addition of ADT. Therefore,
After SRP, 17 patients (22.1%) had erectile dysfunction. Inter- SRP should be considered only for patients with low comorbidity, a
fascial neurovascular bundles preservation was attempted in 11 life expectancy of at least 10 years, a pre-SRP PSA <10 ng/mL and
patients of 51 previously potent. Overall, five patients of 51 (9.8%) biopsy ISUP grade <2/3, no lymph node involvement or evidence of
preserved their erectile function with/without use of PDE-5 in- distant metastatic disease pre-SRP, and those whose initial clinical
hibitors. In the nerve sparing and non-nerve sparing groups, three staging was T1 or T210.
versus two patients preserved erectile function, respectively As robotic surgery techniques for prostate cancer treatment
(p:0.027). progressed, recent series started showing promising improvements
Stratifying patients into robot-assisted versus open approach, regarding functional outcomes in the SRP setting. Until now, sur-
erectile function was conserved in one patient (4.5%) versus four gical outcomes reported in the literature on the open and robotic
(8.7%), respectively (p: 0.540), with the OR in the robot-assisted approach in SRP are limited. In Table 3, the most relevant published
approach of 0.5 (CI 95%: 0.05e4.8, p:0.547). series are compared. To our knowledge, we are the first institution

Please cite this article as: Martinez PF et al., Comparing open and robotic salvage radical prostatectomy after radiotherapy: predictors and
outcomes, Prostate International, https://doi.org/10.1016/j.prnil.2020.07.003
4 Prostate International xxx (xxxx) xxx

Table 2
Perioperative results.

Variable Total (n:76) Open (n:50) Robot-assisted (n:26) p-value

pTNM (%) 0.451

pT2 25 (32.9) 19 (38) 6 (23.1)
pT3a 22 (28.9) 13 (26) 9 (34.6)
pT3b 24 (31.6) 14 (28) 10 (38.5)
pT3b N1 5 (6.6) 4 (8) 1 (3.8)
Gleason sum post-SRP (%) 0.466
7 24 (31.6) 18 (36) 6 (23.1)
8 28 (36.8) 18 (36) 10 (38.5)
9 24 (31.6) 14 (28) 10 (38.5)
Positive SM (%) 22 (28.9) 15 (30) 7 (26.9) 0.779
Rectal injury (%) 1 (1.3) 0 1 (3.8) 0.163
Clavien-Dindo III-V (%) 7 (9.2) 4 (8) 3 (11.5) 0.613
EBL median (IQR), ml 150 (50-350) 200 (50-400) 150 (50-250) 0.122
Transfusion rate (%) 2 (2.6) 2 (4) 0 0.301
HS median (IQR), days 3 (2-4) 3 (2-4) 2 (2-3) 0.127
Catheterization, days, median (IQR) 15 (13-21) 20 (15-21) 13 (11-14) 0.01

SM: surgical margin; pTNM: pathological tumor-node-metastasis; EBL: estimated blood loss; HS: hospital stay. Bold value indicates p-value less than 0.05 is statistically
significant.

Fig. 1. KaplaneMeier survival curves expressing the estimated BCR-free survival rate.

in Latin America in reporting a single tertiary cancer center expe- fibrosis; thus, tissues are frailer, adhesions are more frequent, and
rience in open and robot-assisted SRP and showing improvements healing becomes less effective, altering surgical planes and
in terms of continence and anastomotic stricture. anatomical landmarks, than a nonirradiated pelvis15. As a
RT induces a wide variety of short- to long-term changes in consequence, postoperative complications and UI risk may be
the prostate and surrounding tissues, from neo-angiogenesis to increased in SRP compared with first-line radical prostatectomy,

Table 3
Comparison of published salvage radical prostatectomy series.

Author Year Patients; n Approach BCR % PSM% LN þ, % Overall urinary incontience % Overall anastomotic stricture %

Eandi21 2010 18 Robotic 67 28 5.5 67 17

Heidenreich9 2010 55 Open/lap 87 11 20 19 11
Chade17 2011 404 Open 37 25 16 - -
Zugor22 2014 13 Robotic 46 0 - 46 0
Kenney23 2016 39 Open/robotic 30 15.3 12.8 25.6
Gontero5 2019 395 Open/robotic - - 15.7 42.5 11.85
Present Study 2020 76 Open/robotic 67 28.9 6.6 26.4 8.8

BCR: biochemical recurrence; PSM: positive surgical margin; LNþ: lymph node involved; Lap: laparoscopic.

Please cite this article as: Martinez PF et al., Comparing open and robotic salvage radical prostatectomy after radiotherapy: predictors and
outcomes, Prostate International, https://doi.org/10.1016/j.prnil.2020.07.003
 P.F. Martinez et al. / Comparing open and robotic salvage 5

reflecting the technical challenge and the high surgical Longer follow-up is necessary to estimate CSS and BCR-free
complexity. survival, although many studies reported a 5-year BCR-free sur-
Regarding blood transfusions, only open SRP was associated vival greater than 45%, as in Chade's17 and Mandel's18 series (48%
with an increased requirement (4%), whereas none of the patients and 48.7%, respectively). This correlates with our published data,
in the robotic group had significant blood loss. Recently, Gontero where the estimated 2-year BCR-free survival rate in the open
et al5 published a similar blood transfusion rates, 6.5% versus 2.7% approach group and robot-assisted group was 67% (CI 95%:
in open versus robotic SRP, respectively. 53.7e80.3) and 60.9% (CI 95%: 40.5e81.3), respectively, with no
Vesicourethral anastomosis stricture is one of the most feared statistical difference. In 2014, we observed an estimated 4-year
complications, which needs, in the vast majority of the cases, BCR-free survival of 51.7%, although in this study sample size was
additional surgical procedures, leading sometimes to severe in- smaller with longer follow-up time19. In a systematic review by
continence that can only be controlled with an artificial urinary Matei et al20 on SRP, better biochemical control and CSS rates were
sphincter or urinary diversion12. Series describing functional out- demonstrated with SRP than other salvage therapies. Moreover,
comes of robotic SRP after primary treatment confirm that com- salvage therapy can avoid or defer ADT20.
plications such as anastomotic stricture are frequent, ranging from Based on our published outcomes and when oncologically
11% to 25.6%13 as shown in Table 3. Contrarily, Kaffenberger et al.14 indicated, we consider SRP should not be avoided because of the
reported a lower risk of anastomotic stricture in robotic SRP, fear of poor outcomes18. Contrarily, its use should be recommended
ranging from 0 to 17% versus 11% to 30% in the open approach when we focus to achieve cancer-free status, considering that pa-
group. In our series, we reported a stricture incidence of 8.7%; all of tient selection is of paramount importance.
them occurred in patients who underwent the open approach (p- This study has several strengths. First, median follow-up time
value ¼ 0.07). The surgeon should keep this issue in mind while was reasonable to measure our primary endpoints. Second, out-
performing the suture in these complicated cases. We recommend comes were analyzed and compared in two different surgical
additional catheter days in these patients, to allow full tissue techniques. However, some limitations are worth mentioning. First,
healing before applying tension on the anastomosis. Interestingly, it is a retrospective analysis of prospectively collected data, and
no strictures were identified in the robot-assisted group. We there is a potential selection bias. In addition, because of both the
believe that when performing robotic anastomosis, both the precise small sample size and small number of events, multivariate analysis
alignment between the bladder neck and the urethral stump as was not performed. Further randomized studies are needed to
well as the nonischemic waterproof running suture used in this confirm our findings, and patient selection should be of greatest
step could explain these findings. importance in SRP setting to avoid major surgical complications.
UI continues to be a significant concern after SRP. For example,
Gontero et al5 showed that 57.5% of patients had improved/un- 5. Conclusions
changed continence at the last follow-up at 6 or 12 months whereas
24.6% were severely incontinent. On their multivariable analysis The present study adds important information about contem-
robotic-SRP was an independent predictor for continence preser- porary outcomes of patients undergoing SRP for radiorecurrent
vation (OR: 0.411, CI 95%: 0.232e0.727, p ¼ 0.022). In the present prostate cancer. Open SRP and robot-assisted SRP have similar
study, we observed a UI rate of 34.2% in the open group versus 9.1% oncological outcomes with excellent cancer control. Robot-assisted
in the robotic group, being the overall incontinence rate of 26.4%. SRP is a reliable procedure to treat local recurrences after EBRT or
This is an acceptable outcome, when comparing previous reports BT, reducing the risk of anastomotic strictures and blood loss and
(Table 3). We also found that BT as primary treatment might result improving continence outcomes.
in a UI predictor (OR: 4.8, CI 95%: 1.1e20). Heidenreich et al.9 found
an opposite result as they demonstrated a faster continence re- Conflicts of interest
covery in SRP after BT.
According to recent reviews, erectile function in SRP is poorly All authors have no conflict of interest to declare.
preserved with approximately less than 20% of patients maintain-
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Analysis of the Feasibility and Safety of Salvage Robot-Assisted Radical

Please cite this article as: Martinez PF et al., Comparing open and robotic salvage radical prostatectomy after radiotherapy: predictors and
outcomes, Prostate International, https://doi.org/10.1016/j.prnil.2020.07.003