Impact of a Low-Volume Laparoscopic Radical Prostatectomy Learning Curve on Perioperative Outcomes: Is It Acceptable?

Abstract

Objective:

The reproducibility of high-volume published series of laparoscopic radical prostatectomy (LRP) is still debatable. Many questions about its implementation, safety, and number of procedures required to achieve competence and improvement of outcomes with the technique remain unclear, and a learning curve study is crucial to investigate the acceptable performance of this advanced, minimally invasive procedure.

Subjects and Methods:

Between 2004 and 2011, 240 consecutive patients underwent an LRP performed by a single surgeon and were divided into the first, second, and third groups of 80 patients each. Perioperative and oncologic outcomes were compared across the groups to assess the impact of the learning curve for LRP. All surgical complications were classified using the Clavien–Dindo system (CDS).

Results:

Mean (range) patient age was 61 (43–78) years. The mean (range) level of prostate-specific antigen was 6.47 (3–18) ng/mL. The mean (range) Gleason sum was 6 (5–9). There was a significant reduction in the mean operative time (P<.001), mean anastomosis time (P<.001), mean blood loss (P<.001), mean hospital stay (P<.001), and mean minor CDS complications (P<.01) among the three groups as the series progressed. The D'Amico tumor stage was an independent factor for positive surgical margin across the learning curve (P<.001).

Conclusions:

Our study demonstrated safety and low morbidity of the LRP technique since the beginning of a learning curve development, in which up to 80 cases were necessary to create a plateau to improve faster perioperative parameters, although, from the plateau created, it requires a very large number of surgeries for slightly better, additional overall benefits. In spite of its complexity and steep learning curve, new surgeons can be encouraged in the LRP technique with mentorship training without compromising overall outcomes, permitting the wide spread of an alternative minimally invasive procedure in low-volume centers.

Introduction

Laparoscopic radical prostatectomy (LRP) was first performed in 1991 and published in 1992.¹ Schuessler and Clayman² published the initial series of laparoscopic prostatectomy in 1997, having performed the first case 5 years earlier. The long operative time of 9.5 hours was caused by lack of experience with the procedure and a difficult operative technique, including the anastomosis between the bladder neck and urethral stump.² In the 1990s, Guilloneau and Vallancien³ refined and standardized the technique, publishing good results. The present report documents a low-volume learning curve of the procedure performed by a single laparoscopic surgeon in a Brazilian medical institution and investigates the impact on perioperative outcomes of an alternative and advanced minimally invasive procedure.

Subjects and Methods

From December 2004 through June 2011, 240 consecutive patients underwent LRP for the treatment of clinically localized prostate cancer and were retrospectively evaluated with our hospital database. During this period, all cases were undertaken by one surgeon at the University Hospital Gaffre and Guinle (UNIRIO), besides other private hospitals, in Rio de Janeiro, Brazil. The patients were placed in a supine, modified lithotomy (abducted thighs) position with the arms adducted and the table set in a 15–30° Trendelenburg position. The operative team included the surgeon standing on the left of the patient, a first assistant on the right side of the patient, and a second assistant standing next to the surgeon. Before initiation of the LRP learning curve, the single surgeon had prior open prostatectomy and upper tract laparoscopy experience, as well as prior learning from training with a laparoscopic prostatectomy mentorship.

Preoperative demographic data of the patients, intraoperative parameters (surgical time, bleeding, and complications), and postoperative outcomes (initiation of the oral diet and ambulation, complications, and length of hospital stay) were retrospectively analyzed. Oncological data were assessed by pathological examination, and functional outcomes were assessed up to 6 months after surgery. All complications that occurred within the first 6 months of surgery were recorded, defined, and graded using the Clavien–Dindo system (CDS).

All patients were subjected to a transperitoneal antegrade laparoscopic approach, as previously described in the urological literature.⁴ Vesicourethral anastomosis was performed with 2-0 Monocryl™ (poliglecaprone 25; Ethicon, Somerville, NJ) continuous suture in a clockwise direction starting at 3 o'clock. All knots were tied intracorporeally. The bladder was filled with 120 mL of saline via the catheter to test the integrity of the anastomosis. A Penrose drain was inserted routinely to drain the pelvic region.

For dissection and hemostasis, ultrasonic energy and monopolar diathermy were used in the series, alternating dissection with cold scissors and titanium clips. All patients were routinely typed in the preoperative time for eventual blood transfusion. Ilio-obturator lymphadenectomy was performed only in patients with prostate-specific antigen values of ≥10 mg/mL and a Gleason score of ≥7. A urethral catheter was maintained for 14 days by department routine.

Statistical analysis

Statistical comparison of quantitative variables was accessed by the Kruskal–Wallis nonparametric test. For categorical variables, the chi-squared nonparametric test or Fisher's exact test was used. For all tests, the threshold for statistical significance was set at 5%. Analyses were done using R software (version 2.14.2; http://mirrors.nics.utk.edu/cran/).

Results

Preoperative data

The mean age of the patients was 61 years (range, 43–78). The majority of the patients were classified as American Society of Anesthesiologists I (40.41%) and II (56.67%). Thirty-three cases (13%) had a history of previous surgery. Of these 33 patients, 14 had appendicectomy, 1 had nephrectomy, 3 had a unilateral inguinal hernia, 8 had bilateral inguinal hernias, 1 had an umbilical hernia, 4 had cholecystectomy, 1 had varicocelectomy, and 1 had gastrectomy. All procedures were conventionally performed transperitoneally.

All patients were preoperatively staged with clinically localized adenocarcinoma of the prostate. Most of the patients (80.41%) had a moderate Gleason score (Gleason 3+3), and the mean prostate-specific antigen level was 6.47 ng/mL (range, 3–19 ng/mL). The mean prostate weight evaluated through transrectal ultrasound was 43.6 g (range, 30–150 g). The preoperative patient data are summarized in Table 1.

Table 1.

Preoperative Parameters Stratified by Learning Curve Groups

	Group 1 (Patients 1–80)	Group 2 (Patients 81–160)	Group 3 (Patients 161–240)	Total	P value
Age (years)	62.5 (56.8, 67)	61 (56, 65.2)	60 (56, 67)	61 (56, 67)	.765^a
Mean PSA (ng/mL)	30 (19, 37.2)	28 (19, 36)	30 (19, 36)	29 (19, 36)	.773^a
ASA score					.953^b
I	30 (37.5%)	34 (42.5%)	33 (41.25%)	97 (40.4%)
II	47 (58.75%)	44 (55%)	45 (56.25%)	136 (56.7%)
III	3 (3.75%)	2 (2.5%)	2 (2.5%)	7 (2.9%)
Ultrasound prostate weight	35 (35, 40)	37.5 (35, 45)	35 (35, 50)	35 (35, 45)	.259^a
Clinical stage					.606^b
cT1	46 (57.5%)	44 (55%)	48 (60%)	138 (57.5%)
cT2	29 (36.25%)	33 (41.25%)	30 (37.5%)	92 (38.33%)
cT3	5 (6.25%)	3 (3.75%)	2 (2.5%)	10 (4.17%)
Pathological stage					.91^b
pT2	55 (68.75%)	52 (65%)	58 (72.5%)	165 (68.75%)
pT3	24 (30%)	27 (33.75%)	21 (26.25%)	72 (30%)
pT4	1 (1.25%)	1 (1.25%)	1 (1.25%)	3 (1.25%)
Biopsy Gleason score					.495^c
<6	64 (80%)	62 (77.5%)	67 (83.75%)	193 (80%)
≥6	16 (20%)	18 (22.5%)	13 (16.25%)	47 (20%)

Data are median (interquartile range) values or n (%) as indicated.

P value calculated by Kruskal–Wallis test.

P value calculated by Fisher's exact test.

P value calculated by chi-squared test.

ASA, American Society of Anesthesiologists; PSA, prostate-specific antigen.

Intraoperative data

Only two procedures (0.83%), which were performed in public institutions, could not be concluded via laparoscopy because of technical problems with the gas flow to create the pneumoperitoneum.

On average, the operative time was 175.3 minutes (range, 130–360 minutes). The mean operating time for Group 1 (Patients 1–80) was 207.3 minutes, for Group 2 (Patients 81–160) was 161 minutes, and for Group 3 (Patients 161–240) was 160.3 minutes Figure 1.

FIG. 1.

(a) The overall operative time learning curve. (b) Comparing Groups 1–3 in the operative time leaning curve: the effect of the plateau created near 80 cases (after Group 1 was performed).

On average, the mean anastomosis time was 20.5 minutes (range, 13–75 minutes). The mean anastomosis time for Group 1 (Patients 1–80) was 27.4 minutes, for Group 2 (Patients 81–160) was 18 minutes, and Group 3 (Patients 161–240) was 16.9 minutes Figure 2.

FIG. 2.

(a) The overall anastomosis time learning curve. (b) Comparing Groups 1–3 in anastomosis time leaning curve: the effect of the plateau created near 80 cases (after Group 1 was performed).

For dissection and hemostasis, ultrasonic energy was used in 61 patients, and monopolar diathermy and titanium clips were used in 193 patients. The energy was not used in the typical anatomy prostate neurovascular bundles. In Group 1 (Patients 1–80), 76.25% were performed with ultrasonic energy, whereas only 22.5% were done so for Group 2 (Patients 81–160) and none in Group 3 (Patients 161–240).

The estimated average intraoperative blood loss was 290.4 mL (range, 100–1000 mL). A blood transfusion was needed in 13 cases (5.41%),with a range of blood loss of 654 mL and use of 1–3 blood units. Of these 13 patients, 8 cases received 1 blood unit with a blood loss of 544 mL (range, 400–700 mL), 2 cases received 2 blood units with a blood loss of 750 mL (range, 700–800 mL), 2 cases received 3 blood units with a blood loss of 1000 mL (range, 1000 mL), and 1 case received 7 blood units because of postoperative blood loss (the intraoperative data summary is given in Table 2 and Fig. 3).

FIG. 3.

Boxplot of blood loss, operative duration, and anastomosis time comparing the three learning curve groups: the effect of the plateau created near 80 cases (after Group 1 was performed).

Table 2.

Intraoperative Parameters Stratified by Learning Curve Groups

	Group 1 (Patients 1–80)	Group 2 (Patients 81–160)	Group 3 (Patients 161–240)	Total	P value^a
Operative duration (minutes)	210 (165, 230)	150 (140, 152.5)	150 (140, 150)	150 (150, 210)	.001
Anastomosis duration (minutes)	22.5 (18.8, 35)	20 (15, 20)	15 (15, 20)	20 (15, 20)	.001
Blood loss (mL)	400 (200, 500)	250 (200, 300)	250 (200, 300)	275 (200, 300)	.001

Data are median (interquartile range) values.

P value calculated by Kruskal–Wallis test.

Postoperative data

Regarding postoperative data, oral fluids and diet were introduced as tolerated. All patients initiated diet and ambulation on the first postoperative day. The average length of hospital stay was 2.15 days (between 2 and 5 days).

The overall incidence of postoperative complications was 20.41% (49/240). The incidence of CDS minor complications (Grade I–II) was 39/240 (16.25%). The incidence of CDS major complications (III–V) was 10/240 (4.16%). The complication rates for each group are summarized in Table 3.

Table 3.

Postoperative Parameters Stratified by Learning Curve Groups

	Group 1 (Patients 1–80)	Group 2 (Patients 81–160)	Group 3 (Patients 161–240)	Total	P value
Hospital stay (days)	2 (2, 5)	2 (2, 3)	2 (2, 2)	2 (2, 3)	.001^a
Deambulation (days)	1	1	1		—
Oral fluids and diet (days)	1	1	1		—
CDS complications
Minor	21 (26.25%)	9 (11.25%)	9 (11.25%)	39	.01^b
Major	6 (7.5%)	2 (2.5%)	2 (2.5%)	10	.18^b

Data are mean (interquartile range) values or n (%) as indicated.

P value calculated by Kruskal–Wallis test.

P value calculated by chi-squared test.

CDS, Clavien–Dindo system.

During the immediate postoperative period, 7 patients (2.91%) presented fever without any clinical repercussion. Tachyarrhythmia was observed in 1 patient (0.41%) who needed treatment in the intensive care unit; however, the postoperative evolution was normal. There were 12 cases of prolonged urine drainage that recovered well by prolonged catheterization. The major complication was a recto-urethral fistula with late identification that occurred with the first case of our series; thus it was necessary to perform a colostomy. Afterward, the patient was subjected to surgical correction of the fistula followed by bowel transit reconstruction with a satisfactory recovery. There were 7 cases of bladder neck stenosis requiring endoscopic incision in the postoperative period. There was 1 case of late postoperative blood loss (Day 2) caused by an artery bleeding, needing 7 blood units, that immediately stopped after pudendal artery embolization.

There was no postoperative mortality or readmission to the hospital up to 1 month. The postoperative data are demonstrated in Table 3 and Figure 4.

FIG. 4.

Boxplot of hospital stay comparing learning curve groups: the effect of the plateau created near 80 cases (after Group 1 was performed).

Histology data

The histology data were based on using the 2002 Tumor-Node-Metastasis classification, and we stratified the groups into low, intermediate, and high tumor risk by the D'Amico classification. There were 41 cases of positive surgical margins (PSMs) (17.08%). Stratified by location, we had 16 cases at the apical region, 11 cases at the bladder neck region, and 14 cases at the posterolateral region. Stratified by pathological stage, the PSM rate was 15.15% for pT2 disease, 18.05% for pT3 disease, and 100% for pT4 disease. Tumor stage by the D'Amico classification was an independent factor for PSM across the learning curve (P<.001).

Continence and potency data

At a mean follow-up of 6 months (range, 0.3–8 months) 77.9% (187/240) of patients were completely dry (pad-free); 14.1% (34/240) of patients used between 1 to 2 pads/day, and 8% (19/240) used from 3 to 4 pads/day.

With respect to sexual function, 87% of all cases had moderately good preoperative potency (IIEF-5 score >16, Sexual Health Inventory for Men questionnaire). After 1 and up to 6 months after surgery, satisfactory erections occurred in 127 patients (52.9%). Of these, 54 had spontaneous erections, and 73 could achieve erection with a phosphodiesterase type 5 inhibitor. A further 70 patients used intracavernosal prostaglandin injections to achieve erection. The remaining 43 patients were not interested in sexual rehabilitation and have not had additional treatment.

Discussion

LRP is an advanced surgical procedure with a long initial operative duration, including the urethrovesical anastomosis, which attests this technical difficulty and requires significant laparoscopic expertise.⁵

However, the definition of a learning curve in any surgical procedure is still debatable. Uncertainty exists regarding the number of procedures required to achieve acceptable competence in the procedure. The challenge in developing a new learning curve is, in the first instance, to maintain safety, focused on perioperative parameters such as operative time, blood loss, and complications.⁶ Subsequently, as experience is acquired, improvement of oncologic outcomes such as decreased positive margins of specimens and long-term biochemical recurrence-free survival follow-up are mandatory.^7,8

A few reports in the literature have documented that a faster initial learning curve of about 50–60 cases is needed to facilitate independent operating with acceptable outcomes for surgeons with previous laparoscopic experience.^6–9 Nevertheless, further improvements in operative, oncologic, and functional outcomes can be seen from 250–350 up to 750 cases.^7–10

A large multicenter retrospective study of almost 5000 patients confirmed the high level of experience needed to provide good long-term oncologic outcomes, although no benefit to prior open surgical experience was shown, whereas the learning curve effect was similar between the laparoscopic and open cohort.⁸ Furthermore, more structured practical training including surgical simulation based in laboratories and operating rooms and continuing medical education are necessary to make the gain in learning curve experience faster. In another study, in a learning curve of three surgeons it was demonstrated that prior laparoscopic experience and mentorship allowed dissemination of the complex technique with good short-term results, which highlights the importance of enhanced laboratory laparoscopic skills training and education.¹¹

In another recent comparison of the surgeon's background experience, Frede et al.¹² showed no advantage in prior open prostatectomy. Indeed, for the surgeons with previous laparoscopic experience, the learning curve was shorter, which was also helped by mentorship from pelvic laparoscopists.¹³

In our series, before initiating the LRP curve, the single surgeon, with prior open prostatectomy, had performed several upper tract laparoscopic surgeries such as nephrectomy, adrenalectomy, nephroureterectomy, and pyeloplasty.

Operative total time and anastomosis time decreased as familiarity with the operation increased, which was confirmed after the learning curve of approximately our first 80 cases was performed (Group 1). Our mean operative time was 160 minutes, nearly the same as that for other best reference centers, for which the median data vary between 2 and 4.5 hours.^14,15

Laparoscopy reduces operative blood loss as a result of improved control of the dorsal vein complex combined with the tamponading effect of capnoperitoneum and the excellent view and magnification afforded by the laparoscope, permitting meticulous hemostasis.

The average blood loss and average transfusion rate in this series (265.7 mL; range, 100–1000 mL; in 4.72% of patients) is comparable with values reported in the literature (514 mL; range, 185–1230 mL; in 0%–31% of patients).^16,17 Our results demonstrated a faster performance of the operative time, anastomosis time, and mean blood loss learning curve across the groups (P<.001).

Bipolar electrocautery is associated with a lower risk of tissue injury from an inadvertent energy transfer compared with monopolar diathermy, offering surgeons important benefits including minimal lateral thermal tissue damage, minimal charring, and desiccation.¹⁸ Harmonic^® (Ethicon) technology reduces the need for ligatures with simultaneous cutting and coagulation. Moreover, there is no electricity to or through the patient with greater precision near vital structures, producing minimal smoke with improved visibility in the surgical field. However, there have been a few questionable prospective randomized controlled trials showing the advantages of the Harmonic scalpel compared with monopolar diathermy.¹⁹ In our series, in the first 80 cases, the majority of the cases (86%) were performed with Harmonic diathermy. With the learning curve and experience, monopolar diathermy (not in the neurovascular bundle) and clips were used in 82% of Group 2 (Patients 81–160) and 100% of Group 3 (Patients 161–240), with no statistical difference in mean operative time and estimated blood loss compared with ultrasonic energy. In this manner, our study suggests further investigation about the alternative use of monopolar diathermy in minor centers with no availability of bipolar energy, which could be used by surgeons in the intermediate and advanced learning curve stages in LRP.

The laparoscopic technique has the potential to improve postoperative leakages rates from the urethrovesical anastomosis, as a result of the superior length of the urethral stump, watertight running urethrovesical anastomosis performed under optimal visualization, and meticulous tissue handling and dissection. This was observed in our series in which there was 10% of intraoperative anastomosis leakage in the first 80 cases (Group 1) compared with 2.4% in the total of 240 cases.

A PSM is defined as the extension of the tumor to the inked surface of the resected specimen.²⁰ The status of the surgical margin has been shown to be a reliable predictor of cancer control that can be influenced by the surgical technique, making it a very suitable parameter especially in reports such as ours with a short duration of postoperative follow-up.

Rassweiler et al.²¹ had an overall positive margin rate of 23.7% in their large series, with a range of 15%–44% elsewhere.²² Jacob et al.²³ reported positive margin rates of 18.9% for laparoscopic surgery. In our series, the PSM rate of 17.08% (41 cases) indicates that an apparently satisfactory oncological technique was achieved.

The risk of PSMs is relatively high for the apical and posterolateral regions of the prostate,²⁴ and it can be reduced by increased experience and the learning curve.²⁵

Analyzing the distribution of positive margins in our series, we observed that all the 4 cases of apex margin occurred in the first 20 patients with a localized tumor, which probably could be explained by the early Group 1 learning curve.

There are few studies comparing positive margin rate separately for pT2 and pT3 disease. Pavlovich et al.²⁶ compared open versus laparoscopic versus robotic-assisted techniques and observed that the positive margin rate did not statistically differ for pT2 disease when comparing the three techniques. However, there were higher PSM rates associated with minimally invasive techniques compared with the open procedure when analysis was confined to pT3 disease.²⁵

The explanation in this group for this finding may be that, for locally advanced disease, tactile feedback can provide important information with respect to resection margins and intraoperative decision-making. Another explanation may be related to the learning curve associated with pure and robotic-assisted laparoscopic procedures. In our series, PSM rates were increased from pT2 disease to pT3 disease, whereas all patients with pT4 disease had PSMs, which could be related to the learning curve across the groups with the association of the biological behavior of the tumors. Our study demonstrated that the D'Amico tumor stage was an independent factor for PSM across the learning curve (P<.001).

The hospital stay represents an important part of the cost of radical prostatectomy and is influenced by several factors like age, resumption of feeding, use of peridural anesthesia, and postoperative analgesia.²⁷ Guillonneau and Vallancien²⁸ showed that LRP was less costly than the retropubic approach, mainly because the hospital stay was shorter.

In our series, all the patients resumed oral diet and ambulation after the first postoperative day with a short hospital stay, similar to the literature reports, with statistical significance (P<.001) about the learning curve across the groups.

Laparoscopic prostatectomy has complication rates equivalent to or less than those of open surgery.²⁹ The complications are usually local (rectal injury, urine leakage), whereas Guillonneau et al.^6,28 identified anastomotic leakage as the most common complication (10%). Rectal injury occurs during 1.4%–2.4% of laparoscopic procedures, gastrointestinal lesions in 0.8%–0.93% of transperitoneal procedures, ureteric wounds in 0.7%–0.8%, and epigastric artery damage in 0.5%–2.9%.^6,28,30 Only one major complication, with late identification of a recto-urethral fistula, occurred in the first case of our preliminary series reported,³¹ which attests to the lack of a learning curve to avoid complications. Moreover, our study demonstrated a progressive decrease in major (P<.18) and minor (P<.01) CDS complications across the learning curve groups.

Most of the laparoscopic pure and robotic radical prostatectomy cases are performed in a small number of high-volume centers in Europe and the United States, allowing for intensive learning of a complex procedure.³² However, centralization of prostate cancer care could create unintended barriers and unintentionally limit access to radical prostatectomy for certain populations.³³ Centralization is still debatable, particularly because prostatectomy patients do not have the financial or social means to travel long distances, and loss of surgical cases may jeopardize the economic stability of smaller and community hospitals.^33,34 In this manner, the widespread use of the LRP technique can provide prostatectomy patients with access to an alternative minimally invasive procedure in low-volume centers.

Conclusions

In spite of its complexity and steep learning curve, new surgeons can be encouraged in the LRP technique with mentorship training without compromising overall outcomes, permitting the wide spread of an alternative minimally invasive procedure in low-volume centers.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Schuessler

, Kavoussi

, Clayman

. Laparoscopic radical prostatectomy: Initial case report [abstract] J Urol, 1992; 147:A246.

Schuessler

, Clayman

. Laparoscopic radical prostatectomy: Initial short term experience. Urology, 1997; 50:854–857.

Guillonneau

, Vallancien

. Laparoscopic radical prostatectomy: The Montsouris experience [abstract] J Urol, 1992; 147:A246.

Abreu

, Gill

. Pertinent issues related to laparoscopic radical prostatectomy. Int Braz J Urol, 2003; 29:489–496.

Gill

, Zippe

. Laparoscopic radical prostatectomy: Technique. Urol Clin North Am, 2001; 28:423–436.

Guillonneau

, Rozet

, Cathelineau

, Lay

, Barret

, Doublet

et al. Perioperative complications of laparoscopic radical prostatectomy: The Montsouris 3-year experience. J Urol, 2002; 167:51–56.

Kavoussi

. Laparoscopic radical prostatectomy: Irrational exuberance? Urology, 2001; 58:503–505.

Vickers

, Savage

, Hruza

et al. The surgical learning curve for laparoscopic radical prostatectomy: A retrospective cohort study. Lancet Oncol, 2009; 10:475–480.

Tooher

, Swindle

, Woo

et al. Laparoscopic radical prostatectomy for localized prostate cancer: A systematic review of comparative studies. J Urol, 2006; 175:2011–2017.

10.

Eden

, Neill

, Louie-Johnson

. The first 1000 cases of laparoscopic radical prostatectomy in the UK: Evidence of multiple 'learning curves.' BJU Int, 2009; 103:1224–1230.

11.

Vasdev

, KassLliyya

, Patel

et al. Developing a laparoscopic radical prostatectomy service: Defining the learning curve. J Endourol, 2012; 26:903–910.

12.

Frede

, Klein

, Teber

, Rassweiller

. Laparoscopic radical prostatectomy—Impact of training and supervision. Minim Invasive Ther Allied Technol, 2005; 14:104–108.

13.

Fabrizio

, Tuerk

, Schellhammer

. Laparoscopic radical prostatectomy: Decreasing the learning curve using a mentor initiated approach. J Urol, 2003; 169:2063–2065.

14.

Guillonneau

, Catheliau

. Prostatectomy radical coelioscopique: Première evaluation après 28 interventions. Presse Med, 1998; 27:1570–1574.

15.

Guillonneau

, Catheliau

. Cancer de la prostate localize: Traitement par prostatectomy radical coelioscopique. Etude de 841 cas. Bull Acad Natl Med, 2002; 186:117–123.

16.

Rassweiler

, Stolzenburg

, Sulser

, Deger

, Zumbé

, Hofmockel

et al. Laparoscopic radical prostatectomy: The experience of the German Laparoscopic Working Group. Eur Urol, 2006; 49:113–119.

17.

Hasan

, Gill

et al. Laparoscopic radical prostatectomy. BJU Int, 2004; 94:7–11.

18.

McKernan

, Stuto

, Champion

. New application of bipolar coagulation in laparoscopic surgery. Surg Laparosc Endosc, 1996; 6:335–340.

19.

Catena

, Ansaloni

, Di Saverio

, Gazzotti

, Coccolini

, Pinna

. The HAC Trial (Harmonic for Acute Cholecystitis) Study. Randomized, double-blind, controlled trial of Harmonic (H) versus monopolar diathermy (M) for laparoscopic cholecystectomy (LC) for acute cholecystitis (AC) in adults. Trials, 2009; 10:34.

20.

Watson

, Civantos

, Soloway

. Positive surgical margins with radical prostatectomy: Detailed pathological analysis and prognosis. Urology, 1996; 48:80–90.

21.

Rassweiler

, Seemann

, Schulze

et al. Laparoscopic versus open radical prostatectomy: A comparative study at a single institution. J Urol, 2003; 169:1689–1693.

22.

Rassweiler

, Tsivian

, Kumar

et al. Oncological safety for urological malignancy: Experience with more than 1,000 operations. J Urol, 2003; 169:2072–2075.

23.

Jacob

, Salomon

, Hoznek

, Bellot

, Antiphon

, Chopin

, Abbou

et al. Laparoscopic radical prostatectomy: Preliminary results. Eur Urol, 2000; 37:615–620.

24.

Salomon

, Anastasiadis

, Levrel

et al. Location of positive surgical margins after retropubic, perineal and laparoscopic radical prostatectomy for organ confined prostate cancer. Urology, 2003; 61:386–390.

25.

Katz

, Salomon

, Hoznek

et al. Positive surgical margins in laparoscopic radical prostatectomy: The impact of apical dissection, bladder neck remodeling and nerve preservation. J Urol, 2003; 169:2049–2052.

26.

Magheli

, Gonzalgo

, Su

L-M

et al. Impact of surgical technique (open vs laparoscopic vs. robotic-assisted) on pathological and biochemical outcomes following radical prostatectomy: An analysis using propensity score matching. BJU Int, 2010; 107:1956–1962.

27.

Gardner

, Bissonette

, Petroni

et al. Surgical and postoperative factors affecting length of hospital stay after radical prostatectomy. Cancer, 2000; 89:424–430.

28.

Guillonneau

, Vallancien

. Laparoscopic radical prostatectomy: The Montsoris experience. J Urol, 2000; 163:418–422.

29.

Salomon

, Hosnek

. Radical retropubic versus laparoscopic prostatectomy: A prospective comparison of functional outcome. Urology, 2003; 62:292–297.

30.

Hoznek

, Salomon

et al. Laparoscopic radical prostatectomy: The Créteil experience. Eur Urol, 2001; 40:38–45.

31.

Rubinstein

, Barros

. Laparoscopic radical prostatectomy: Preliminary report. Bras J Video Surg, 2008; 1:64–66.

32.

, Gu

, Lipsitz

et al. Comparative effectiveness of minimally invasive vs open radical prostatectomy. JAMA, 2009; 302:1557–1564.

33.

Stizenberg

, Wong

, Nielsen

, Egleston

, Uzzo

. Trends in radical prostatectomy: Centralization, robotics, and access to urologic care. Cancer, 2012; 118:54–62.

34.

Lowrance

, Elkin

, Jacks

et al. Comparative effectiveness of prostate cancer surgical treatments: A population based analysis of postoperative outcomes. JAMA, 2009; 302:1557–1564.