Robot-Assisted Radical Prostatectomy in Patients with a History of Holmium Laser Enucleation of the Prostate: The Indiana University Experience

Abstract

Introduction:

We sought to update our experience of oncologic and functional outcomes of robot-assisted radical prostatectomy (RARP) for prostate cancer in patients with history of holmium laser enucleation of the prostate (HoLEP).

Patients and Methods:

Twenty-seven patients with previous HoLEP who underwent RARP were matched 1:1 with RARP patients with no history of transurethral surgery. Demographic, operative, oncologic, continence, and erectile function outcomes were analyzed.

Results:

Median time between HoLEP and RARP was 31 months with a mean prostate-specific antigen doubling time of 4.28 ng/mL/year. Operative times were significantly longer with higher bladder neck reconstruction rates and similarly low complication rates. Biochemical recurrence was relatively low (7%) in the HoLEP group, identical to the comparative group. Continence at last follow-up was not statistically significant between groups, although time to continence favored the non-HoLEP cohort. Erectile function recovery was generally poor in the post-HoLEP cohort (11%), although bilateral nerve sparing was rarely performed (11%). Compared with our initial experience, there were significant improvements in time to continence (16 vs 36 weeks). No T2 post-HoLEP RARP since 2010 has had a positive surgical margin.

Conclusions:

Post-HoLEP prostatectomy remains feasible with similar perioperative and oncologic outcomes compared with matched cohorts. Functional recovery remains slowed yet may continue to improve with technical familiarity.

Introduction

There are a number of open and minimally invasive surgical options for benign prostatic hyperplasia (BPH).^1,2 Although transurethral resection of the prostate (TURP) is a more common intervention than holmium laser enucleation of the prostate (HoLEP), HoLEP has been shown to be effective for lower urinary tract symptoms, especially for prostate volumes larger than 50 g.³ Both procedures allow for pathologic detection of prostate cancer in a small but consistent percentage of patients.^4

–7 Although many of these patients can be safely managed with active surveillance initially, a portion will ultimately require primary therapy where robot-assisted radical prostatectomy (RARP) could be considered.^8,9

Management of prostate cancer with open radical prostatectomy following TURP has been described as challenging but feasible.¹⁰ RARP has been shown to provide perioperative advantages in these patients; however, RARP has been shown to be more difficult than in transurethral-naive patients.^11
–13 Nerve-sparing radical prostatectomy after HoLEP has been described with mixed results.¹⁴ Our initial series of RARP after HoLEP published in 2015 focused on our first 11 patients and described feasibility of the technique and preliminary functional and oncologic outcomes.¹⁵ The objective of this study was to update our experience with a larger cohort of patients with longer follow-up. We also sought to assess whether the surgeon learning curve with the procedure improved our initial results.

Patients and Methods

Patient selection

Between 1998 and 2018, 2626 patients were identified in our institutional review board (IRB) database, who underwent HoLEP using previously described techniques at Indiana University.¹⁶ Inclusion criteria were prior HoLEP for BPH, pathologically diagnosed prostate cancer on HoLEP specimen or subsequent post-HoLEP TRUS biopsy, and RARP performed at our institution. We identified 27 men who met the criteria for evaluation. Nearly 75% of the cohort had HoLEP performed by a single surgeon (J.E.L.) and 75% underwent robotic prostatectomy performed by a single surgeon (R.S.B.). Patients were matched 1:1 to patients undergoing RARP without a history of HoLEP or any transurethral surgery. Matching criteria included biopsy Gleason score, pre-RARP prostate-specific antigen (P.S.A.) level (within 2 ng/mL), and age (within 2 years).

Surgery

RARP was performed (M.O.K. and R.S.B.) in a standard manner.^17,18 Additional technical nuances of the bladder neck and apical dissection related to anatomical changes associated with prior HoLEP were described in our original analysis and applied to our contemporary cohort.¹⁵ No patients undergoing post-HoLEP RARP underwent a posterior dissection. Nerve sparing (unilateral or bilateral) was performed in 48% of patients at surgeon's discretion based on preoperative pathologic information, preexisting erectile function, and surgical tissue planes. Lymph node dissection was performed in 89% of patients and included removal of obturator and external iliac lymph node packets.

Following prostatectomy, patients were routinely followed at 6 weeks, 3, 6, 9, and 12 months for the first year, then biannually for an additional year, and then annually. The majority of patients who received nerve-sparing surgery were placed immediately on daily low-dose tadalafil for 3 months and transitioned to a higher dose if needed. Additional adjunctive therapy such as a vacuum erectile device or injection therapy was utilized upon request.

Outcomes

Primary outcomes of interest for this updated analysis of RARP after HoLEP were oncologic (margin status, extraprostatic extension, biochemical, and recurrence-free survival) and functional (urinary and erectile domains). RARP pathology was reviewed and compared between groups. These included Gleason score, surgical margins, capsular extension, seminal vesicle invasion (SVI), and positive lymph nodes.

Urinary continence was evaluated both through the American Urological Association (AUA) symptom score and urinary pad usage. Our definition of functional urinary continence was leak free at the most recent follow-up, with the allowance of a single security pad. We also analyzed “strict continence,” which was defined as leak free and pad free at the most recent follow-up. Time to continence outcomes were based on our functional continence definition. Potency was evaluated via both sexual health inventory for men (SHIM) score and the ability to achieve an erection with aid of phosphodiesterase-5 inhibitors or vacuum-assisted devices.

Statistical analysis

Descriptive statistics were utilized to analyze outcomes. t-Tests for differences in means and Mann–Whitney tests were utilized for normally and non-normally distributed continuous variables, respectively. Pearson χ ² and Fisher's exact tests were used for categorical variables. Statistical tests were performed two sided with a significance level of p < 0.05. IBM SPSS version 24 software was used in statistical analysis.

Results

Overall median follow-up of the 27 patients undergoing prior HoLEP RARP was 20 months (range: 1–98). More than 70% had at least 1 year of follow-up. Characteristics of HoLEP patients are presented in Table 1. Fourteen patients (52%) were cancer free following HoLEP, while 13 (48%) had cancer detected at time of HoLEP. Gleason-grade group scores ranged from Gleason-grade group 1 (69%) to Gleason-grade group 5 (8%). Average time from HoLEP to RARP was 58 months (nearly 5 years) ranging from 2 months to more than 13 years. Prostate-specific antigen (PSA) at the time of HoLEP, PSA nadir following HoLEP, and PSA kinetics leading to RARP are shown as well.

Table 1.

Patient Demographics, HoLEP, and PSA Data in Post-HoLEP Patients Undergoing Robot-Assisted Radical Prostatectomy

Characteristic	HoLEP patients (N = 27)
Age at HoLEP (years), mean (SD)	64.8 (6.2)
HoLEP time (minutes), median (IQR)	60 (44)
Volume resected (g), mean (SD)	68.2 (55.6)
Cancer in HoLEP, n (%)	13 (48)
Age at radical prostatectomy (years), mean (SD)	69.6 (5.1)
Time to prostatectomy (months), median (IQR)	31 (71)
Pre-HoLEP PSA (ng/mL), mean (SD)	9.10 (6.39)
PSA nadir (ng/mL), mean (SD)	2.25 (2.54)
PSA velocity (ng/mL/year), mean (SD)	4.28 (3.82)

HoLEP = holmium laser enucleation of prostate; IQR = interquartile range; PSA = prostate-specific antigen; SD = standard deviation.

Of patients who had cancer in their specimen, 8 of 13 (62%) underwent transrectal ultrasonography biopsy, whereas five proceeded to prostatectomy between 1 and 14 months following HoLEP. Of the 14 patients with benign HoLEP specimen, 12 underwent prostate biopsy before prostatectomy due to rising PSA and two secondary to a palpable nodule on digital rectal examination.

Preoperative characteristics before RARP for both HoLEP patients and their matched controls are shown in Table 2. No differences were seen between groups in age, body mass index, PSA, biopsy Gleason scores, and potency and continence at baseline. PSA density was greater in the HoLEP group nearing statistical significance, and clinical staging frequencies were statistically different with matched controls having mainly T1c tumors. Baseline continence levels were similar in both groups, and while potency rates were greater in the HoLEP-naive cohort, this difference did not reach significance.

Table 2.

Preoperative Characteristics

	Post-HoLEP (N = 27)	HoLEP-naive (N = 27)	p
Age (years), mean (SD)	69.5 (5)	67.6 (4)	0.086
BMI (kg/m²), mean (SD)	28.0 (4.3)	29.6 (3.8)	0.157
PSA (ng/mL), mean (SD)	5.78 (2.6)	5.36 (2.05)	0.672
PSA density (ng/mL²), mean (SD)	0.164 (0.094)	0.116 (0.061)	0.057
Clinical stage, n (%)			0.056
T1a	3 (15)	0 (0)
T1b	2 (10)	0 (0)
T1c	13 (65)	22 (81)
T2a	2 (10)	4 (15)
T2b	0 (0)	1 (4)
Gleason-grade group pre-RARP, n (%)			0.877
1	3 (11)	5 (18)
2	14 (52)	16 (59)
3	2 (7)	3 (11)
4	4 (15)	2 (7)
5	1 (4)	1 (4)
Baseline potent, n (%)	7 (37)	14 (67)	0.059
Baseline continent, n (%)	23 (85)	26 (96)	0.159

BMI = body mass index; RARP = robot-assisted radical prostatectomy.

In Table 3, perioperative findings are demonstrated. Operative duration was greater in the HoLEP group (193.5 vs 164.2 minutes, p < 0.001), however, no difference was seen in blood loss. There were two complications recorded in our HoLEP cohort and none in the matched controls, although this difference was not significant. Reported complications were nonurologic: an emergent hemorrhoidectomy for rectal bleeding and an infiltrated intravenous leading to a second-degree burn treated conservatively. Nerve-sparing outcomes were significantly different between our two groups with more than half of patients in the control group receiving bilateral nerve sparing compared with only three patients in the HoLEP group (p = 0.002). Rates of bladder neck repair during anastomosis were significantly greater in post-HoLEP patients as well (39% vs 11%, p = 0.029).

Table 3.

Perioperative and Postoperative Outcomes of Patients Undergoing Robot-Assisted Radical Prostatectomy

	Post-HoLEP (N = 27)	HoLEP-naive (N = 27)	p
Operative time (minutes), mean (SD)	193.5 (43.4)	164.2 (34.1)	<0.001
Estimated blood loss (mL), mean (SD)	160 (93)	130 (62)	0.322
Estimated blood loss (mL), median (IQR)	100 (150)	100 (50)	0.784
Complications, n (%)	2 (7)	0 (0)	0.491
Nerves spared, n (%)			0.002
0	14 (52)	12 (44)
1	10 (37)	2 (7)
2	3 (11)	14 (52)
Bladder neck repair, n (%)	11 (39)	3 (11)	0.029
Gland size (g), mean (SD)	40.3 (20.7)	53.3 (21.7)	0.004
Gleason-grade group (pathologic), n (%)			0.337
1	4 (15)	2 (7)
2	13 (48)	20 (74)
3	6 (22)	4 (15)
4	0 (0)	0 (0)
5	3 (11)	1 (4)
Positive surgical margins, n (%)	6 (22)	5 (18)	0.735
Extracapsular extension, n (%)	13 (48)	14 (52)	0.785
Seminal vesicle invasion, n (%)	4 (15)	1 (4)	0.351
Lymphovascular invasion, n (%)	4 (14)	0 (0)	0.038
Positive lymph nodes, n (%)	2 (7)	2 (7)	1.000
Time to catheter removal (days), mean (SD)	8.3 (2.0)	7.8 (1.9)	0.370
Length of hospitalization (days), median (IQR)	1 (0)	1 (0)	0.418
Potent at last follow-up, n (%)	3 (11)	7 (29)	0.305
Functional continence (0–1 pad/day), n (%)	16 (59)	22 (81)	0.156
Strict continence (pad free/leak free), n (%)	6 (22)	20 (74)	<0.001
Time to continence (months), median (IQR)	20 (24)	6 (13)	0.007
Most recent AUA symptom score, mean (SD)	7.1 (7.0)	8.0 (7.2)	0.556
Most recent SHIM score, mean (SD)	2.7 (1.8)	13.5 (5.7)	<0.001
Biochemical recurrence, n (%)	2 (7)	2 (7)	1.000
Continence-related surgery, n (%)	3 (11)	2 (7)	1.000
Follow-up (weeks), median (IQR)	20 (48)	24 (35)	1.000

AUA = American Urological Association; SHIM = sexual health inventory for men.

Pathologic outcomes are displayed in Table 3. Patients without a history of transurethral surgery had larger prostate glands (53.3 vs 40.3 g, p = 0.004) at the time of RARP. While there were more Gleason-grade group 3 and higher in the post-HoLEP group, these differences were not statistically significant (p = 0.337). While similar between cohorts, it should be noted that positive surgical margins were found in our initial three post-HoLEP prostatectomy patients and then subsequently were not identified in any pathologic T2 patients. Locations of positive margins in the post-HoLEP group included the left posterior apex, right posterior apex, right anterior apex, and the left periseminal vesicle region in a patient with T3b disease. Extraprostatic extension, SVI, and positive nodal status frequencies were similar between analyzed cohorts.

Functional outcome comparisons between both groups are listed in Table 3. Mean AUA symptom scores were not significantly different between groups, although a significant difference in the last reported SHIM score existed. Rates of potency and functional continence at most recent follow-up were similar between experimental cohort and matched controls. Time to continence was significantly greater in our HoLEP group (20 vs 6 months, p = 0.007). Of note, some patients in the original series have since achieved continence, and all patients had greater follow-up data leading to differences in statistics between the analyses. Of the four patients who did not have functional continence recovery following HoLEP before radical prostatectomy, only one achieved functional continence following RARP.

Follow-up times were similar between groups, and rates of patients requiring continence-related surgery were not significantly different. Two prior HoLEP patients underwent artificial urinary sphincter (AUS) surgery, while one received a urethral sling, similar to the controls (one AUS and one sling). Rates of biochemical recurrence were similarly low at last follow-up (8% vs 7%, p = 1.000).

Comparison of our initial series of post-HoLEP RARP published in 2015 and our more recent experience is listed in Table 4. Our analysis demonstrates improvements in surgical and functional outcomes for patients over time. Operative time and blood loss are significantly reduced in our more recent series. Regarding oncologic outcomes, we have been able to achieve 100% margin negativity rates for organ confined disease in our more recent series. Overall margin rates and biochemical recurrence rates have remained similar and encouraging since our initial analysis. In patients achieving functional continence, we found that time to continence was reduced from an average of 36–16 weeks (p = 0.006).

Table 4.

Comparison of Initial Series of Robot-Assisted Radical Prostatectomy Patients with Updated Cohort

	Initial series (N = 11)	Updated series (N = 16)	p
Operative time (minutes), mean (SD)	216.7 (59.5)	177.6 (15.7)	0.018
Estimated blood loss (mL), mean (SD)	209 (99)	127 (74)	0.031
Estimated blood loss (mL), median (IQR)	200 (150)	100 (106)	0.054
Complications, n (%)	0 (0)	2 (12.5)	0.499
Positive surgical margins, n (%)	2 (18)	4 (25)	1.000
Potent at last follow-up, n (%)	3 (27)	0 (0)	0.228
Time to continence (weeks), median (IQR)	36 (11)	16 (16)	0.006
Biochemical recurrence, n (%)	1 (9)	1 (6)	1.000
Continence-related surgery, n (%)	1 (9)	2 (13)	1.000
Follow-up (weeks), median (IQR)	66 (37)	11.5 (24)	0.021

Discussion

The results herein further demonstrate the feasibility of RARP following HoLEP. The present study confirms many initial findings from our previously published case series.¹⁵ First, this operation is safe and reproducible and outcomes improve with increasing experience. Our present results demonstrate that learning curves exist for RARP in this cohort, even in experienced surgeons. Second, oncologic outcomes are similar and noninferior to robotic prostatectomy in transurethral-naive patients. Finally, while improved from our initial series of patients, continence and potency after RARP are negatively impacted by the previous HoLEP. Our updated analysis continues to underscore that RARP after prior HoLEP remains viable for clinically significant prostate cancer, although with certain considerations.

Other groups have previously evaluated feasibility and outcomes of prostatectomy in patients with previous BPH surgery. It is suggested that radical prostatectomy (whether open or robotic) after previous prostate surgery can be performed safely, although with some detrimental effects on functional recovery. Colombo and colleagues evaluated 109 men who underwent open radical prostatectomy over 4 years, who had previous surgery for bladder outlet obstruction (88 TURP, 21 simple prostatectomy). These surgeries were associated with longer operative times and worse functional outcomes when compared with treatment-naive men.¹⁰ Another study performed a matched-pair analysis to determine if RARP or open radical prostatectomy was superior in men who underwent TURP. Margin rates were similar; however, blood loss, transfusion rates, complications, and length of hospital stay were superior in the RARP cohort. Long-term functional and oncologic outcomes were not assessed.¹¹ Reports regarding the feasibility of radical prostatectomy, whether open or robotic, following HoLEP are limited. Suardi and colleagues performed a 1:1 matched study of 15 men who underwent open nerve-sparing radical prostatectomy following HoLEP to men who underwent nerve-sparing radical prostatectomy after TURP or open prostatectomy. Interestingly, surgical margin status was better in men who previously underwent HoLEP. No functional outcome differences were seen between groups at follow-up of almost 2 years.¹⁴

Our previous report of our initial experience of 11 men undergoing post-HoLEP RARP and the present expanded study corroborate many of these findings. We demonstrate that even with history of HoLEP, patients can expect similarly low blood loss, hospitalization lengths, and complication rates as their naive counterparts. Our present study suggests that although functional outcomes are clearly inferior to treatment-naive patients, knowledge of surgical anatomy and surgeon experience help mitigate detrimental effects on urinary continence and erectile function.

While we do not know of groups that have looked at RARP outcomes after HoLEP, Suardi and colleagues have reported on nerve-sparing open radical retropubic prostatectomy after HoLEP and compared them with patients undergoing identical surgery after TURP or simple prostatectomy.¹⁴ They too found post-HoLEP procedure challenging but described encouraging early functional and surgical outcomes. By nature of our practice patterns, we focused on robotic rather than open radical prostatectomy and elected to match patients with no history of transurethral surgery rather than patients who underwent prior TURP. In our initial series, we reported encouraging preliminary results with the understanding that functional outcomes may not be identical to naive patients.¹⁵ With longer follow-up and an expanding group of post-HoLEP RARP patients, we report here updated outcomes for this population that further suggest feasibility of this procedure.

The results of this study must be viewed in the context of certain limitations. As a retrospective study there is implicit selection bias that is acknowledged. Our study group remains relatively small, which could impact generalizability of our results. However, our report continues to represent the largest group of post-HoLEP robotic radical prostatectomy reported on in the literature. Given that many of our patients are referred in for their BPH surgery (and in many cases their RARP), some data points were unavailable and routine follow-up, PSA screening, and biopsy schedules were not standardized. Follow-up post-RARP, however, was standardized as previously outlined. As such, continence and erectile function following surgery were recorded in 3–6-month time intervals; therefore, functional recovery may have been achieved sooner than documented. Finally, some men who developed prostate cancer, at or after time of HoLEP over this period, elected for nonsurgical therapies (radiation, active surveillance, and hormonal therapy). These men were not included in the present analysis; however, we are currently reviewing these data and initiating a multi-institutional study to evaluate different treatment options for localized prostate cancer in men who have undergone prior HoLEP surgery.

These limitations notwithstanding, we believe the results of the present study demonstrate that RARP after HoLEP is a sound reproducible operation for patients. Operative times, complication rates, and oncologic results have been consistently satisfactory and are nearly identical to our compared cohort. This should give confidence to both surgeons and patients who undergo HoLEP and are diagnosed with clinically significant prostate cancer during follow-up. Overall continence and leak-free pad-free states fall short of radical prostatectomy in non-HoLEP patient endpoints, and time to plateau takes significantly longer. Optimal time for RARP may partly depend on recovery of continence following HoLEP. Erectile function, while hard to quantify in this cohort because of poor initial potency and low frequency of bilateral nerve-sparing procedures, also appears to be inferior, stressing the critical importance of appropriate counseling for patients to understand the pluses and minuses of taking on a second major prostate operation.

Conclusions

In patients with a history of HoLEP who develop prostate cancer, RARP provides a challenging yet sound and reproducible surgical option. Margin status and rates of disease recurrence appear unaffected by previous enucleation. Time to continence, while improved with increased experience, remains overall inferior to standard comparison. Few patients retain viable erections without assistance in the post-HoLEP RARP setting. These patients should be uniquely counseled about these considerations when considering radical prostatectomy for clinically significant prostate cancer.

Footnotes

Author Disclosure Statement

Dr. James E. Lingeman is a consultant with Boston Scientific, Beck Laboratories, and Lumenis.

Funding Information

There is no funding for this article.

Abbreviations Used

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