Functional outcomes following robotic prostatectomy using athermal, traction free risk-stratified grades of nerve sparing
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- Tewari, A.K., Ali, A., Metgud, S. et al. World J Urol (2013) 31: 471. doi:10.1007/s00345-012-1018-7
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To report our unique approach for individualizing robotic prostate cancer surgery by risk stratification and sub classification of the periprostatic space into 4 distinct compartments, and thus performing 4 precise different grades of nerve sparing based on neurosurgical principles and to present updated potency and continence outcomes data of patients undergoing robotic-assisted laparoscopic prostatectomy (RALP) using our risk-stratified approach based on layers of periprostatic fascial dissection.
Patients and methods
(1) Between January 2005 and December 2010, 2,536 men underwent RALP by a single surgeon at our institution. (2) Included patients were those with ≥1-year follow-up and were preoperatively continent and potent, defined as having a SHIM questionnaire score of >21; thus, the final number of patient in the study cohort was 1,335. (3) Postoperative potency was defined as the ability to have successful intercourse (score of ≥4 on question 2 of the SHIM); continence was defined as the use of no pads per 24 h.
(1) The potency and continence for NS grades 1, 2, 3, and 4 were found to be 90.6, 76.2, 60.5, and 57.1 % (P < 0.001) and 98, 93.2, 90.1, and 88.9 % (P < 0.001), respectively. (2) The overall PSM rates for patients with NS grades 1, 2, 3, and 4 were 10.5, 7, 5.8, and 4.8 %, respectively (P = 0.064).
The study found a correlation between risk-stratified grades of NS technique and continence and potency. Patients with lesser grades of NS had higher rates of potency and continence.
KeywordsProstate cancerNerve sparingRobot-assisted laparoscopic radical prostatectomyContinencePotency
Prostate cancer is the most common non-dermatologic cancer affecting men in the Western World . With more than 60 % of radical prostatectomies (RP) being robot-assisted laparoscopic prostatectomy (RALP), it has largely replaced the standard primary treatment option of open retro pubic radical prostatectomy as a surgical treatment option for prostate cancer [2, 3]. The well-established adverse effects of urinary incontinence and sexual dysfunction still persist and have a significant impact on Health Related Quality of Life (HRQoL) . Widespread usage of PSA as a screening test has resulted in earlier detection and diagnosis of prostate cancer in younger men and has further necessitated the importance of postoperative recovery of genitourinary functions. Our previously described risk-stratified technique is based on neuroanatomical findings [5, 6] with the goals of achieving functional outcomes without compromising the oncological safety . We also have previously found a correlation between risk-stratified grade of nerve sparing (NS) technique and early return of urinary continence . Postoperative potency and continence rates are used as a benchmark for functional outcomes following RP. Potency outcomes are dependent on many factors such as patient’s age, type and extent of nerve sparing, and pre-operative erectile function [9–11]. While return of urinary continence has been found to be dependent on factors such as patient demographics, presence of median lobe, degree of nerve sparing, and changes in surgical technique [12–14].
Prostate cancer surgery involves interplay between competing goals of cancer extirpation, nerve sparing, postoperative recovery of urinary continence, and potency. The margin of error is very small, and at no time cancer cells are more than few mm away from important nerves and sphincteric muscles. The peri-prostatic space is 3–5 mm tissue comprising of nerves, vessels, lymphatics, ganglions, fat, loose areolar, and connective tissue condensed as fascial layers. Sometimes smooth or skeletal muscle fibers are also present in this space. Few years ago the discussion about nerve sparing was a binary decision—nerve sparing or non-nerve sparing. Surgeons usually differentiated left and right sides as distinct entities, and thus, 3 different scenarios were possible—bilateral nerve sparing, bilateral non-nerve sparing, or unilateral nerve sparing. Over last several years, due to the efforts by many investigators [2, 6, 15–23] and due to improved magnification, we now know that nerve sparing could be an incremental process, and even if we suspect extra prostatic extension (EPE) (in low grade cancers) we can still save lateral nerves while removing inner peri-prostatic tissue and thus achieving the oncological goal. This risk-stratified approach allows more nerves to be preserved in increasing number of patients while maintaining oncological efficacy of this procedure. This evolution in our thought process was the foundation for this work. The key developments were as follows: (a) pre-operative risk stratification allowing us to group patients in 4 (rather than 2) groups with incremental risk in incidence of EPE [7, 24], (b) anatomic studies clarified the peri-prostatic space anatomy and also established that these nerves are organized as a hammock of interconnected nerves, ganglions, arteries, and veins , (c) the anatomic studies also clarified that nerves are mostly lateral to the veins and capsular arteries which can serve as landmark during surgery [17, 26], (d) the use of high resolution, 3 T multi-parametric MRI(Magnetic Resonance Imaging) with endorectal coil for risk stratification and study of peri-prostatic space and surgical planning in patients when not contraindicated . Based on our studies involving correlation between pre-operative imaging, risk stratification, intra-operative finding, and ability to dissect 3–5 mm of peri-prostatic space into three distinct fascial planes, we were able to develop the grades of nerve sparing approach and collect data regarding oncological and functional outcomes in a large cohort of patients [6–8, 17, 24–26]. Nerve sparing Robotic prostatectomy is actually a combination of oncological and neurosurgical operation that requires precision, delicateness, and adjustments to match patients unique parameters.
We have previously published our initial results, and this present study involves our extended cohort and combined results on margin, sexual function, and continence in 1,335 preoperatively potent and continent patients with ≥1-year follow-up operated at our institution by a single surgeon (AKT).
Patients and methods
The data collection of baseline variables was collected under an institutional review board-approved protocol concerning HRQoL for patients undergoing RALP at our institution. The baseline continence at follow-up intervals was assessed using the question, “How many pads or adult diapers per day did you usually use to control leakage during the last 4 weeks?” Continence was defined as use of 0 pads per 24 h. Postoperative potency was defined as the ability to have successful intercourse (score of ≥4 on question 2 of the SHIM) with or without the use of PDE5 inhibitors. All patients received the SHIM questionnaires to assess their pre-operative sexual function.
A follow-up questionnaire was dispatched to patients through either post or electronic mail at 6, 12, 26, and 52 weeks after RALP. The subjects were contacted by telephone at each of the follow-up intervals to ensure receipt of the questionnaire. Data collection and follow-up correspondence were performed by a third-party (not involved in patient care) in compliance with the Health Insurance Portability and Accountability Act (HIPAA).
Postoperative potency was defined as the ability to have successful intercourse (score of ≥4 on question 2 of the SHIM) with or without the use of PDE5 inhibitors.
All patients were recommended penile rehabilitation; patients were advised to use phosphodiesterase type 5 inhibitors at least three times per week until sexual function recovery.
Statistical analysis was performed using PASW version 20.0 (SPSS, Inc., Chicago, IL, USA). Categorical distributions are reported as counts (percentages), and continuous variables are reported as medians and interquartile ranges. The Pearson’s chi-square test was used to analyze categorical variables. The Kruskal–Wallis test was used to assess continuous variables. Univariate and Multivariate logistic regression models were constructed to identify predictors of continence. All tests were two sided with statistical significance with a P < 0.05.
Pathologic data collection
Examination of pathologic specimens for presence or absence of positive surgical margin (PSM) and extra prostatic extension (EPE) was done by dedicated genitourinary pathologists. The specimen handling and fresh tissue banking were done in accordance with our previously published protocol .
Grade 1 NS: The Denonvilliers’ fascia and the later pelvic fascia (LPF) are incised just outside the prostatic capsule to preserve the neural hammock. We also describe this as medial venous plane for complete hammock preservation. This is the greatest degree of NS possible, and we perform this procedure for patients with no-to-minimal risk of EPE.
Grade 2 NS: The Denonvilliers’ fascia (leaving deeper layers on the rectum) and LPF are incised just outside the layer of veins of the prostate capsule. This allows the preservation of most large neural trunks and ganglia and is used for patients at low risk of EPE.
Grade 3 NS (partial/incremental): Incision is made through the outer compartment of the LPF (leaving some yellow adipose and neural tissue on the specimen), excising all layers of Denonvilliers’ fascia. This is performed for patients with moderate risk of EPE because some of the medial trunks are sacrificed, whereas the lateral trunks are preserved.
Grade 4 NS (non-NS): These patients have high risk of EPE and are not candidates for NS. In such cases, we perform a wide excision of the LPF and Denonvilliers’ fascia containing most of the peri-prostatic neurovascular tissue. In selected patients, we attempt nerve advancement of the identifiable ends of the neurovascular bundles (NVB).
Patients with different NS grades on each side of the prostate are classified according to the higher NS grade (lesser NS) of the two in the present study.
Baseline demographics, clinical and pathological data of 1335 patients with ≥1-year follow-up and pre-operative SHIM >21
n = 1,335
Age (median, IQR)
BMI (median, IQR)
Pre-operative PSA (median, IQR)
Pre-operative SHIM (median, IQR)
Prostate volume (median, IQR) %
Clinical stage (%)
Biopsy Gleason (%)
7 (3 + 4)
7 (4 + 3)
Pathology Gleason (%)
7 (3 + 4)
7 (4 + 3)
Pathology stage (%)
LN + (%)
Positive surgical margin (%)
Potency outcomes in patients with preoperative SHIM scores of > 21 and with ≥1 year follow-up (n = 1335)
Nerve sparing grade
Potency outcomes in patients with preoperative SHIM scores of >21, aged ≤60 years and with ≥1 year follow-up (n = 858)
Nerve sparing grade
There was a statistically significant difference across the different NS grades for the percentages of patients who achieved continence postoperatively (P < 0.001). Continence was achieved by 98 % NS grade 1 patients, 93.2 % NS grade 2 patients, 90.1 % NS grade 3 patients, and 88.9 % NS grade 4 patients (Table 2; Fig. 6). When only patients aged ≤60 years were considered, the percentages of patients that were postoperatively continent were 98.4, 93.7, 95.8, and 87.2 % for NS grade 1, 2, 3, and 4, respectively (P < 0.001) (Table 3; Fig. 7).
Univariate and multivariate analysis of continence outcomes
OR (CI 95 %)
OR (CI 95 %)
Pathology prostrate volume
The overall PSM rates for patients with NS grade 1, 2, 3, and 4 were 10.5, 7, 5.8, and 4.8 %, respectively (P = 0.064); the EPE rates were 10.9, 14.5, 27.3, and 31.7 %, respectively (P < 0.001). The PSM rates for patients aged ≤60 years were 10, 7.4, 5.2, and 7.7 % for grades 1, 2, 3, and 4, respectively, as given in table.
The anatomic basis of preservation of nerves was first described by Walsh . The bladder, ureter, seminal vesicles, prostate, urethra, and corpus cavernosum are innervated by visceral branches from the pelvic plexus, which is formed by parasympathetic fibers originating from the ventral rami of S2, S3, and S4 and sympathetic fibers from thoracolumbar center (T11–L2). Recent studies have suggested that the course of the NVBs is more complex than previously described by Walsh . Costello et al.  established that most of the NVB’s descend posteriorly to the seminal vesicles, converge at mid-prostatic level, and then diverge again as they approach the prostate apex. In 2006, Tewari et al.  demonstrated that the periprostatic nerves consistently fall into three broad surgically identifiable zones: the proximal neurovascular plate (PNP), the predominant neurovascular bundle (PNVB), and the accessory neural pathways (ANP) in a study on 10 fresh and two fixed cadavers. This architecture of nerves was termed as “Trizonal Neural hammock”. Also, Tewari et al. described the presence of smaller nerves surrounding the prostate with a hammock like distribution, located in periprostatic space and Denonvilliers’ fascia . The neural hammock on which the prostate rests has also been described in other studies . Eichelberg et al. showed that around 20–25 % of nerves were found outside the posterolateral NVB along the ventral circumference of prostate . Also, 3D computer-assisted anatomic dissection has described the course and distribution of periprostatic nerves . These studies have resulted in a better anatomical understanding and development of surgical techniques to preserve the periprostatic nerves and improve the functional outcomes while preserving the oncological goals after RP.
Post-operative recovery of erectile function has been found to be independently associated with age, baseline SHIM score, and nerve sparing . Different modifications of NS technique have been described. Ahlering et al. described that cautery-free NS significantly improved return of sexual function . Menon et al.  described ‘veil of Aphrodite’ technique in which dissection of prostatic fascia is carried to the prostatic surface, and the peri-prostatic tissue is released in a relatively avascular plane. Chien et al.  described clipless antegrade nerve sparing. Our risk-stratified approach to athermal, traction free nerve sparing during RALP reports that increased NS corresponds to increased percentages of patients with post-operative recovery of potency. The effort to balance oncological safety with functional outcomes through the risk-stratified approach can be evaluated through analysis of PSM and EPE rates. PSM rates in our study were not significantly higher with increased NS, while potency outcomes increased. The overall PSM was reported to be 13 % by Menon et al.  for patients undergoing standard NS on both sides (42 %), unilateral ‘veil of Aphrodite’ with contralateral NS (25 %), and bilateral incremental NS (33 %). In our study, patients who underwent NS grade 1 had a potency rate of 92.4 % and a PSM rate of 10.5 %. Moreover, the increase in EPE rates from NS grades 1–4 supports the validity of the risk-stratified approach described in the present study.
Published continence rates at 12 months post robot-assisted radical prostatectomy ranges from 84 to 97 % . The findings of our study show that urinary continence recovery is shown to have a relationship to degree of nerve sparing. We defined continence as patients with 12-month follow-up post RALP and are pad free. Overall the continence rates increase as NS increase as follows: NS grade 1—98 %, NS grade 2—93.2 %, NS grade 3—90.1 %, and NS grade 4—88.9 %. Patient demographics must also be considered when assessing postoperative continence, namely patient age, which is the one demographic factor most commonly linked to continence [12–14]. Our study shows that precise athermal, traction free nerve sparing technique, and age are independent predictors of urinary continence.
Novara published a study examining the predictors of urinary continence in patients who underwent RALP. Multivariable analysis showed that only patient age and Charlson co-morbidity index were significantly associated with 12-month continence status, while only a non-statistically significant trend was noted for patient BMI . There is some controversy over whether nerve preservation results in improvement of urinary incontinence [32, 33]. Our findings are in contrast to this prior publication by Pick et al. Our risk-stratified approach to nerve sparing contributes to continence; however the exact mechanism remains unclear. First, an appreciation of the neural complex and anatomy is necessary in understanding the mechanisms of erection and urinary continence. Correlating the anatomical understanding with functional outcomes has shown that preservation of nerves results in improved continence rates post RALP. The efferent and afferent nerves of the NVB may function in continence restoration. The impact of autonomic innervation on the urethral sphincter was demonstrated by intra-operative stimulation of the NVB, and this resulted in a significant increase in urethral pressure. The sensation of urine entering the membranous urethra causes a spinal reflex and voluntary contraction of the sphincter that will increase the tone of the external urethral sphincter and pelvic floor, and this sensation can improve urinary continence . Surgical technique may also influence continence . There should be minimal use of cautery in the area of the seminal vesicles, to avoid injury to cavernosal nerves. An accurate dissection of the prostatic apex preserving puboprostatic ligaments, sphincter, membranous urethra, neural hammock, cavernosal nerves, and bladder neck has been proposed to improve continence recovery in patients who undergo RP .
The strength of the present study is that it is a single institution and a single surgeon analysis series. However, our study is not without limitations. The continence and potency outcomes of the present may be influenced by the extensive experience of the surgeon, and thus, the results cannot be generalized. Further, continence outcomes were evaluated in a selected cohort with no erectile dysfunction preoperatively, and therefore, selection bias cannot be precluded.
The current study reports and reconfirms a correlation between risk-stratified grade of NS neurosurgical technique and postoperative recovery of potency and continence, as patients with lowest grade of NS had higher rates of recovery of potency and continence without compromising oncological safety.
Conflict of interest
Dr. Ashutosh Tewari discloses that he is the principal investigator on research grants from Intuitive Surgical, Inc. (Sunnyvale, California, USA) and Boston Scientific Corporation; he is a non-compensated director of Prostate Cancer Institute (Pune, India) and Global Prostate Cancer Research Foundation; he has received research funding from, The LeFrak Family Foundation, Mr. and Mrs. Paul Kanavos, Craig Effron & Company, Charles Evans Foundation and Christian and Heidi Lange Family Foundation.