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- Review -

Recent neuroanatomical studies on the neurovascular bundle of the prostate and cavernosal nerves: clinical reflections on radical prostatectomy

Selcuk Yucel, Tibet Erdogru, Mehmet Baykara

Department of Urology, Akdeniz University School of Medicine, Kampus 07070, Antalya, Turkey

Abstract

The neurovascular bundle of the prostate and cavernosal nerves have been used to describe the same structure ever since the publication of the first studies on the neuroanatomy of the lower urogenital tract of men, studies that were prompted by postoperative complications arising from radical prostatectomy. In urological surgery every effort is made to preserve or restore the neurovascular bundle of the prostate to avoid erectile dysfunction (ED). However, the postoperative potency rates are yet to be satisfactory despite all advancements in radical prostatectomy technique. As the technology associated with urological surgery develops and topographical studies on neuroanatomy are cultivated, new observations seriously challenge the classical teachings on the topography of the neurovascular bundle of the prostate and the cavernosal nerves. The present review revisits the classical and most recent data on the topographical anatomy of the neurovascular bundle of the prostate and cavernosal nerves and their implications on radical prostatectomy techniques. (Asian J Androl 2005 Dec; 7: 339-349)

Keywords: prostate cancer; cavernosal nerves; neurovascular bundle; neuroanatomy; prostatectomy; laparoscopy; robotics; nerve graft; penile erection

Correspondence to: Dr Selcuk Yucel, MD, Department of Urology, Akdeniz University School of Medicine, Kampus 07070, Antalya, Turkey.
Tel: +90-242-227-4480, Fax: +90-242-227-4482
E-mail: syucel@akdeniz.edu.tr
Received 2005-02-24 Accepted 2005-06-22
DOI: 10.1111/j.1745-7262.2005.00097.x

1 Introduction

Today, we are more eager than we were in the past to identify patients with more localized disease so that we can give them a chance of an almost curative treatment. Radical prostatectomy offers an effective curative treatment in selected patients [1-5] but is still associated with significant postoperative morbidities, including erectile dysfunction (ED) and urinary incontinence [6-10]. Nerve sparing techniques for anatomic radical prostatectomy developed by Walsh et al. [11-16] and others [17-21] have helped minimizing complications related to nerve injuries. However, the results regarding potency preservation from centers worldwide published in the urological literature are yet to be satisfactory.

Postoperative potency can be influenced by many factors, including preoperative erectile function, patient age, level of disease, surgeon’s experience and interpersonal anatomic variations. The proper identification and preservation of the neurovascular bundle of the prostate and cavernosal nerves on both sides has a pivotal role in maintaining the preoperative erectile function. As the number of centers of excellence for radical prostatectomy have grown, more papers, chapters, excellent drawings and monographs on the topography of the neurovascular bundle have been published [11-13]. However, the potency preservation rates are far from being excellent. Recently, robotic/laparoscopic radical prostatectomy has emerged, claiming better rates as a result of the use of magnified imaging during surgery [22-37]. Despite this, some uncertainty remains on the topographical anatomy of the neurovascular bundle and the cavernosal nerves and this is hampering the outcome of robotic/laparoscopic radical prostatectomy.

Another promising technique that has emerged in recent years involves the nerve grafting of the distal and proximal ends of the neurovascular bundle [38-45] that have been severed because of disease-specific or technical reasons. Unfortunately, despite very delicate and surgically successful nerve anastomosis, nerve grafting also has not lived up to expectations regarding maintenance of potency [41,43-45]. Unsuccessful nerve grafting outcomes have again shifted attentions to the topographical neuroanatomy of the neurovascular bundle of the prostate and the cavernosal nerves. Gross anatomic dissections [46-48] have developed into histological studies that aim to define the cavernosal nerves’ origin and destination [49-56]. Different novel techniques including serial histological sections on adult and fetal tissues, immunohistochemical studies on histological sections to differentiate very fine nerves, and three-dimensional computerized reconstructions of images based on serial histological sections are also utilized to revalidate our classical knowledge of the cavernosal nerves and their interaction with surrounding structures [57-60]. In this study, recent advancements in neuroanatomical studies of the neurovascular bundle of the prostate and the cavernosal nerves was reviewed.

2 Pelvic plexus

The pelvic splanchnic nerves arise from the anterior sacral roots, with most originating from S4 and a few branches from S2 and S3. These parasympathetic fibers from the pelvic splanchnic nerves congregate with sympathetic fibers from the hypogastric nerve to form the pelvic plexus (Figure 1) [50].

The pelvic plexus is located retroperitoneally on both lateral sides of the rectum. The pararectal fascia and perirectal adipose tissue separates the lateral surfaces of the rectum from the pelvic plexus. The pelvic plexus pattern shows a high interpersonal anatomical variation. Each ganglion at the pelvic plexus contains about 20 nerve cell bodies. The superior part is arbitrarily called the vesical plexus and the inferior part, the prostatic plexus. The pelvic plexus can extend as far as 1.5 cm-2.0 cm posterior to the dorsal edge of the rectum and 1.0 cm-1.5 cm superior to the rectovesical pouch (pouch of Douglas). Only histologic sections allow us to define the projections of pelvic plexus since it is very hard to identify the neural tissue amount and mass in the projections in macroscopic adult male anatomic dissections.

The pelvic plexus is intimately associated with the branches of the inferior vesical vein and artery. These vessels are particularly close to the lateral surfaces of the pelvic plexus (Figure 2). Nevertheless, adipose and connective tissue dissections show distinct separable layers of nerves and vessels posteriorly.

However, there are three surgically sound major projections from the pelvic plexus: 1) anterior, extending across the lateral surfaces of the seminal vesicles and infero-lateral surface of the bladder; 2) antero-inferior, extending to the prostatovesical junction and obliquely along the lateral surfaces of the prostate; 3) inferior, running between the rectum and posterolateral surface of the prostate. It is the inferior that is known as the neurovascular bundle of the prostate [49,50,55,61-64] (Figure 1).

There are many cross-communications between these major projections and the pelvic plexus on both sides of the rectum. These connections mostly run within the fascial layer and their physiologic significance has not been clarified yet [49,50,57,59,60,62-65]. For urological purposes, the inferior projection from the pelvic plexus and its connections to the pelvic plexus are especially important. Particular caution is needed when an incision of the posterior bladder neck is made. Because the pelvic plexus is very close, overzealous dissection of the posterior bladder neck may put some pelvic, vesical or prostatic plexus fibers at risk [65].

The control of the lateral pedicles of the prostate is a precarious step because the pelvic plexus lies postero-laterally (Figure 2). When performing this step, staying very close to the prostate surface may help to avoid neural damage [66]. Vattikuti Institute (Henry Ford Hospital, 2799 West Grand Boulevard, Detroit, MI 48202, USA)claims that robotic/laparoscopic radical prostatectomy may be associated with a lower risk to the pelvic plexus because this is the only technique that allows for an antegrade approach (dissection beginning from the prostate base) to the dissection of the prostate surface [65].

3 Neurovascular bundle of the prostate and cavernosal nerves

Before the studies done by Walsh and Donker [46] on fetal specimens, the cause of ED after radical prostatectomies was not well understood. By tracing the autonomic innervation of the corpora cavernosa, Lepor et al. [47] showed that ED can occur secondary to injury to the cavernosal nerves. Classically, it was thought that these nerves branched from the pelvic plexus and ran as a plexus of small nerves within a prominent neurovascular bundle on the posterolateral border of the prostate, before piercing the urogenital diaphragm and descending along the lateral aspect of the urethra. They are intimately associated with capsular vessels of the prostate and they course outside the prostatic capsule [11-15,47,48,67,68]. These initial findings have since been supported by additional anatomic studies, which have further characterized the anatomy of the neurovascular bundle of the prostate. Detailed histological studies have revealed the cross-sectional profile of the neurovascular supply of the prostate and have shown that it runs through leaves of the lateral pelvic fascia. Even-tually, the cavernosal nerves and the neurovascular bundle of the prostate have been used to describe the same neural structures.

New advancements in surgery, including the use of laparoscopic/robotic modalities and magnifying visual devices in open surgery, have enabled very precise nerve dissection. Nerve grafting and interposition to realign the neurovascular bundle after neurovascular bundle resections are now offered to patients to restate their potency [38-45]. However, despite all these advancements in nerve preservation or restoration, potency rates have remained unsatisfactory [41,43-45]. Therefore, the classical knowledge of the neurovascular bundle of the prostate and the cavernosal nerves was challenged and revisited. It has been suggested that the neurovascular bundle of the prostate may not cover all of the cavernosal nerves and these unidentified nerves may be severed inadvertently during surgery [49,50,62].

To assist with our understanding of the neuroanatomy of the prostate area, we should be familiar with the fascias and their locations. Generally, the neural structures are covered with the fasciae around the prostate. Simply, the inferior extension of the pelvic plexus unites with several vessels to form a prominent neurovascular bundle of the prostate. The neurovascular bundle of the prostate descends along the postero-lateral border of the prostate. It extends laterally to the junction of the lateral pelvic fascia and pararectal fascia, and posteriorly to the dorsal layer of Denonvilliers’ fascia, which forms a thick fibrous sheath separating the prostatic capsule from the rectum. Laterally and posteriorly, it is continuous with the pararectal fascia, and anteriorly with lateral pelvic fascia. The pararectal fascia extends along the lateral surface of the rectum, while the lateral pelvic fascia separates the levator ani musculature from the lateral surface of the prostate. At the prostatic midline, Denonvilliers’ fascia exists as a single sheet, and widens laterally. At the junction of these three fasciae there are many fibrous tissue layers. The posterior and lateral aspects of the neurovascular bundle run through these layers. Deno-nvilliers’ fasciae and the pararectal fasciae are separated from the anterior and lateral surfaces of the rectum by perirectal adipose tissue that shows a high degree of anatomic variation in amount [18,30,37,49,50,59,62,69] (Figures 3 and 4).

More recently, there have been observations that re fute the dogma that the cavernosal nerve is always within the neurovascular bundle of the prostate [49,50, 62, 64,65] (Figure 5). Proximally, the pelvic splanchnic nerve has a nice spray-like arrangement instead of appearing as a prominent thick bundle. Cavernosal nerves originate from the pelvic splanchnic nerve and course along the most caudal margin of the pelvic plexus not contained within the neurovascular bundle. At the level of the prostatovesical junction, thick identifiable branches originating from the pelvic splanchnic nerves do not reach the dorso-lateral margin of the bladder and prostate to form the prominent neurovascular bundle. Rather, they originate from the hypogastric nerves from the dorso-superior direction and course along the lateral aspect of the seminal vesicles.

At the level or just below the prostatovesical junction some nerves run around and along the dorsal aspect of the prostate but they do not form a fascicle. Although the hypogastric nerve is a part of the sympathetic nervous system, hypogastric nerve branches contain ganglion cell clusters comprising autonomic ganglia at superior levels, for example, around the ureter [70]. Below this area, there is no surgically identifiable thick nerves to reach the dorso-lateral area of the prostate. This obvious gap in nerve supply extends almost 1 cm along the cranio-caudal axis except for several thin nerves that run from the dorso-lateral aspect of the prostate.

Right below this level, vascular structures appear at the dorso-lateral margin of the prostate. The lateral pelvic fascia covers these vascular structures. However, nerve components along these vessels are far fewer than those running dorsal and lateral to the vascular bundle. Thus, the neurovascular bundle does not appear to contain terminal components at this level. Instead, it is accompanied dorso-laterally by extra nerves.

In other words, the plexus of nerves running within the neurovascular bundle branch from the postero-inferior aspect of the pelvic plexus are inferior to the level of the tip of the seminal vesicles (Figure 2). On branching from the pelvic plexus these nerves are spread significantly, with up to 3 cm separating the most anterior and most posterior nerves. The nerves located most anteriorly are intimately associated with the seminal vesicle, coursing along the posterolateral surface, while the nerves located posteriorly run dorsal to the posterolateral verge of the seminal vesicle. Generally, most of the neurovascular bundle descends posteriorly to the seminal vesicle. The nerves converge en route to the mid-prostatic level, forming a more condense neurovascular bundle, only to diverge once again when approaching the prostatic apex [49, 50,62,64] (Figure 6).

Therefore seminal vesicles are an important step in radical prostatectomy. The posterior surface of the seminal vesicle is not vascularized and a surgical plane between the posterior layer of the Denonvilliers’ fascia, and the seminal vesicle could be easily developed. Vessels often approach the seminal vesicle laterally and there is often one artery traveling on the anterior surface of the seminal vesicle between the superficial layers of Denonvilliers’ fascia. In dissection, the key is to get to the surface of the seminal vesicles and avoid dissecting outer layers. Sharp dissection instead of coagulation should be preferred in this area [71]. The bulk of the pelvic plexus and its main branches are located laterally and posteriorly to the seminal vesicles. Therefore, the seminal vesicles should be used as an intraoperative landmark to avoid injuring the pelvic plexus. Some believe that because the neurovascular bundle is very close to the tip of the seminal vesicle, an initial dissection behind the bladder leaves a bloodless area to ease the neurovascular bundle dissection [25,27,34,72]. However, Tewari et al. [65] claim that laparoscopic or robotic surgery enables very delicate dissection of the seminal vesicle without prior retrovesical dissection. Another point to note relates to the traction of the seminal vesicle during surgery. Excessive traction of the seminal vesicle may tether the branches from the pelvic plexus medially. Thus, vessels should be controlled on the seminal vesicle to avoid the risk of injuring nerves [65].

The nerves running in the neurovascular bundle innervate the corpora cavernosa, rectum, prostate, and levator ani musculature. The last three also receive a vascular supply from vessels coursing in the neurovascular bundle. Artery and nerve branches supply the anterolateral wall of the rectum from the prostatic apex to the mid-prostate level. Nerves running in the neurovascular bundle pass through slit-like openings in the lateral pelvic fascia to innervate the superior and middle sections of the levator ani. Many nerve and vascular branches pierce the lateral pelvic fascia distally to supply the inferior portion. The nerves innervating the posterior aspect of the prostate are intimately associated with the capsular arteries and veins of the prostate. These structures penetrate the prostatic capsule along its base, mid-portion and apex [49,50,62, 64].

The constituents of the neurovascular bundle of the prostate are organized into three functional compartments. The neurovascular supply to the rectum is generally in the posterior and postero-lateral sections of the neurovascular bundle, running within the leaves of Denonvilliers’ fasciae and the pararectal fasciae. The levator ani neurovascular supply is in the lateral section of the neurovascular bundle, descending along and within the lateral pelvic fascia. The cavernosal nerves and the prostatic neurovascular supply descend along the posterolateral surface of the prostate, with the prostatic neurovascular supply most anterior. Part of this anterior compartment runs ventral to Denonvilliers’ fascia. The functional organization of the neurovascular is not absolute, and is less pronounced proximally at the levels of the seminal vesicles and the prostatic base. In addition to the nerves descending within the neurovascular bundle, a scattering of nerves extends from the medial margin of the neurovascular bundle to the prostatic midline. The deepest nerves innervate the anterior surface of the rectum at the level of the prostatic apex. The more superficial nerves descend posterior to the prostatic apex and merge laterally with the neurovascular bundle [49, 50,62,64] (Figure 7).

Nerve graft interposition from the sural nerve after neurovascular bundle removal has recently been offered by Kim et al. [38]. However, the report they compiled after a 1-year-long follow-up revealed that successful vaginal penetration had occurred in only 33 % of patients [41,43]. Takenaka et al. [49] developed the nerve graft interposition technique by adding intraoperative electrical stimulation to clearly identify the cavernosal nerve. Unfortunately, they also admit that their success rate is no higher than that of Kim et al. [38]. These recent elegant neuroanatomical studies may enlighten these disappointing results. Takenaka et al. [49, 62] observed that they did the cranial end anastomosis to the hypogastric nerve branches rather than the pelvic splanchnic nerve branches in human fresh cadavers. But how can then be a 30% success rate if anastomosis is performed to hypogastric nerve branches? They thought that the hypogastric nerve in men contained sympathetic and parasympathetic elements. Finally, they recommended intraoperative electrical stimulation in the dorsal, lateral, and caudal areas (including the surgically created neurovascular bundle) for the best cranial anastomosis.

Recently, there has been much ongoing research into how to define cavernosal nerve mapping by intraoperative electrical stimulation [39,44,73-82]. This is particularly important in understanding the interpersonal cavernosal nerve topographical variations. Surgical dissection of the cavernosal nerve can be even more troublesome at the prostate apex than at the cranial end. Takenaka et al. [49,62] observed that the surgically defined neurovascular bundle is often likely to differ from the actual axial course of the cavernosal nerve passing through the pararectal space and the rectourethral muscle. They identified a statistically significant interindividual variation of the topography of the cavernosal nerve at the apex of the prostate (three of eight cadavers). They stated that if we approach the apex of the prostate histologically in three different axes, namely frontal, sagittal and axial, we would observe interindividual variations. For example, a frontal course shows a relatively stable path at the 9-10 o’clock positions. However, sagittal and axial sections showed a shift from the 7-8 o’clock to the 10-11 o’clock position of the cavernosal nerves at the apex of the prostate.

Another critical finding in the recent neuroanatomical studies is the rectourethralis muscle and its close association with cavernosal nerves [59,60,62] (Figure 8). In the retropubic radical prostatectomy, rectourethral muscle should be incised near the apex to protect the nerves passing through the muscle mass (Figure 9). While managing the rectourethralis muscle, every effort should be taken to not put excessive traction on the muscle through the urethral catheter or use forceps to preserve the nerves. Some studies indicated that nerve-sparing approaches could obtain a better continence rate [83-85]. Therefore, Strasser et al. [53] proposed that the neurovascular bundle could contain motor and/or autonomic nerves to the rhabdosphincter. However, recent detailed neuroanatomical studies concluded that these two nerves follow separate courses and that the somatic nerve is a different intra-pelvic nerve while the autonomic nerve is in the neurovascular bundle [18,59,60].

Terada et al. [86] reported that the neurovascular bundle was macroscopically severed on 16 sides, and that a positive intracavernous pressure increase after intraoperative electrical stimulation was detected in five cases. This can be explained by the recent neuroanatomical finding that showed that the cavernous nerve is not contained in the neurovascular bundle. In fact, it is located in the fascia, so deep that some non-nerve-sparing surgeries may result with inadvertent nerve-sparing surgery [87]. On the other hand, a very delicate nerve-sparing procedure could end with ED, because the proxi mal or distal ends could be damaged. Bhandar et al. [61] proposed a different approach for robotic/laparoscopic radical prostatectomy that did not involve opening the periprostatic fascia, thus leaving all small cavernosal nerves intact within the fascia. They called the neurovascular bundle and cavernosal nerves the "veil of Aphrodite" and developed a technical modification to the nerve sparing procedure that spared the main neurovascular trunk, but dissected a wide band of periprostatic fascia extending from the reflection from the pelvic fascia proximally, puboprostatic ligaments distally, Denonvilliers’ fascia posteriorly and free edge anteriorly.

The cavernosal nerves and several small vessels pierce the urogenital diaphragm posterolateral aspect of the membranous urethra, before penetrating the posterior aspect of the corpora cavernosa. Right around the penile hilum, there are some intercommunicating branches between the dorsal nerve of the penis and the cavernosal nerves. It is hypothesized that there is a redundant neural system to maintain the erectile function when cavernosal nerves are severed (Figure 10). However, the functional significance of these intercommunicating branches has not been studied and this hypothesis has yet to be confirmed [55,57,62].

Although neurovascular bundle dissection techniques have been developed in recent years along with advancements in laparoscopic/robotic assisted radical prostat-ectomy, the ideal energy source for dissection is still lacking. Open surgery advocates the avoidance of electrosurgical or ultrasonic energy sources but laparoscopic/robotic assisted surgical techniques are very much dependent on them. In a recent study by Ong et al. [71], electrosurgical or ultrasonic hemostasis energy source related thermal injury to cavernosal nerves has been reported to jeopardize erectile function in a canine model. They have also developed an alternate method for the use of ultrasonic shears in conjunction with a fine-angled clamp, which keeps the active element away from the critical structures. Therefore, apart from advancements in surgical neuroanatomy, refinements in the making of surgical instruments also appear to have contributed to the improved success rates of radical prostatectomies.

Acknowledgment

The present paper was supported by the Akdeniz University Scientific Research and Project Unit. The authors would like to thank Dr Laurence S. Baskin and Baskin Lab’s Research Fellows: Dr Wen Hui-Liu, Dr Carlos Ramon Torres Jr, Dr Guang-Hui Wei, Dr Zhong Wang and Dr Antonio Parreira Euclides de Souza Jr., for their contribution to this research. We also would like to thank Dr Jens Rassweiller for his mentorship in laparoscopic urologic surgery and for reviewing this manuscript.

References

1 Walsh PC, Partin AW, Epstein JI. Cancer control and quality of life following anatomical radical retropubic prostatectomy: results at 10 years. J Urol 1994; 152 (5 Pt 2): 1831-6.

2 Walsh PC. Radical prostatectomy for localized prostate cancer provides durable cancer control with excellent quality of life: a structured debate. J Urol 2000; 163: 1802-3.

3 Walsh PC. Cancer surveillance series: interpreting trends in prostate cancer - part I: evidence of the effects of screening in recent prostate cancer incidence, mortality, and survival rates. J Urol 2000; 163: 364-5.

4 Han M, Partin AW, Pound CR, Epstein JI, Walsh PC. Long-term biochemical disease-free and cancer-specific survival following anatomic radical retropubic prostatectomy. The 15-year Johns Hopkins experience. Urol Clin North Am 2001; 28: 555-65.

5 Han M, Partin AW, Piantadosi S, Epstein JI, Walsh PC. Era specific biochemical recurrence-free survival following radical prostatectomy for clinically localized prostate cancer. J Urol 2001; 166: 416-9.

6 Fischetti G, Cuzari S, De Martino P, Musy M, Valentini MA, Leone P, et al. [Postprostatectomy erectile dysfunction]. Minerva Urol Nefrol 2001; 53: 185-8.

7 Fischetti G, Cuzari S, De Martino P, Musy M, Valentini MA, Fralioli A, et al. [Incidence and treatment of postprostatectomy urinary incontinence. Personal experience]. Minerva Urol Nefrol 2001; 53: 179-83.

8 Chang SS, Peterson M, Smith JA Jr. Intraoperative nerve stimulation predicts postoperative potency. Urology 2001; 58: 594-7.

9 Hotta H, Miyao N, Masumori N, Takahashi A, Sasamura K, Kitamura H, et al. [A clinical study of radial prostatectomy]. Nippon Hinyokika Gakkai Zasshi 1996; 87: 760-5.

10 Miyao N, Adachi H, Sato Y, Horita H, Takahashi A, Masumori N, et al. Recovery of sexual function after nerve-sparing radical prostatectomy or cystectomy. Int J Urol 2001; 8: 158-64.

11 Walsh PC, Lepor H, Eggleston JC. Radical prostatectomy with preservation of sexual function: anatomical and pathological considerations. Prostate 1983; 4: 473-85.

12 Eggleston JC, Walsh PC. Radical prostatectomy with preservation of sexual function: pathological findings in the first 100 cases. J Urol 1985; 134: 1146-8.

13 Schlegel PN, Walsh PC. Neuroanatomical approach to radical cystoprostatectomy with preservation of sexual function. J Urol 1987; 138: 1402-6.

14 Walsh PC. Nerve sparing radical prostatectomy for early stage prostate cancer. Semin Oncol 1988; 15: 351-8.

15 Quinlan DM, Epstein JI, Carter BS, Walsh PC. Sexual function following radical prostatectomy: influence of preservation of neurovascular bundles. J Urol 1991; 145: 998-1002.

16 Steiner MS, Morton RA, Walsh PC. Impact of anatomical radical prostatectomy on urinary continence. J Urol 1991; 145: 512-4.

17 Stenzl A, Colleselli K, Poisel S, Feichtinger H, Pontasch H, Bartsch G. Rationale and technique of nerve sparing radical cystectomy before an orthotopic neobladder procedure in women. J Urol 1995; 154: 2044-9.

18 Steiner MS. Anatomic basis for the continence-preserving radical retropubic prostatectomy. Semin Urol Oncol 2000; 18: 9-18.

19 Myers RP. Practical surgical anatomy for radical prost-atectomy. Urol Clin North Am 2001; 28: 473-90.

20 Huland H. [Morphologic principles for radical prostatectomy]. Urologe A 1991; 30: 361-8.

21 Huland H, Noldus J. An easy and safe approach to separating Denonvilliers' fascia from rectum during radical retropubic prostatectomy. J Urol 1999; 161: 1533-4.

22 Abbou CC, Salomon L, Hoznek A, Antiphon P, Cicco A, Saint F, et al. Laparoscopic radical prostatectomy: preliminary results. Urology 2000; 55: 630-4.

23 Binder J, Kramer W. Robotically-assisted laparoscopic radical prostatectomy. BJU Int 2001; 87: 408-10.

24 Binder J, Kramer W. Telerobotic minimally invasive procedures in urology-laparoscopic radical prostatectomy. Surg Technol Int 2002; 10: 45-8.

25 Gill IS, Zippe CD. Laparoscopic radical prostatectomy: technique. Urol Clin North Am 2001; 28 (2): 423-36.

26 Gill IS, Kerbl K, Clayman RV. Laparoscopic surgery in urology: current applications. AJR Am J Roentgenol 1993; 160: 1167-70.

27 Guillonneau B, Rozet F, Barret E, Cathelineau X, Vallancien G. Laparoscopic radical prostatectomy: assessment after 240 procedures. Urol Clin North Am 2001; 28: 189-202.

28 Rassweiler J, Frede T, Seemann O, Stock C, Sentker L. Telesurgical laparoscopic radical prostatectomy. Initial experience. Eur Urol 2001; 40: 75-83.

29 Rassweiler J, Sentker L, Seemann O, Hatzinger M, Rumpelt HJ. Laparoscopic radical prostatectomy with the Heilbronn technique: an analysis of the first 180 cases. J Urol 2001; 166: 2101-8.

30 Rassweiler J, Marrero R, Hammady A, Erdogru T, Teber D, Frede T. Transperitoneal laparoscopic radical prostatectomy: ascending technique. J Endourol 2004; 18: 593-9.

31 Erdogru T, Teber D, Frede T, Marrero R, Hammady A, Seemann O, et al. Comparison of transperitoneal and extraperitoneal laparoscopic radical prostatectomy using match-pair analysis. Eur Urol 2004; 46: 312-9.

32 Schuessler WW, Schulam PG, Clayman RV, Kavoussi LR. Laparoscopic radical prostatectomy: initial short-term experience. Urology 1997; 50: 854-7.

33 Schulam PG, Link RE. Laparoscopic radical prostatectomy. World J Urol 2000; 18: 278-82.

34 Turk I, Deger IS, Winkelmann B, Roigas J, Schonberger B, Loening SA. [Laparoscopic radical prostatectomy. Experiences with 145 interventions]. Urologe A 2001; 40: 199-206.

35 Menon M, Shrivastava A, Tewari A, Sarle R, Hemal A, Peabody JO, et al. Laparoscopic and robot assisted radical prostat-ectomy: establishment of a structured program and preliminary analysis of outcomes. J Urol 2002; 168: 945-9.

36 Menon M, Tewari A, Peabody J. Vattikuti Institute prost-atectomy: technique. J Urol 2003; 169: 2289-92.

37 Menon M, Tewari A, Peabody JO, Shrivastava A, Kaul S, Bhandari A, et al. Vattikuti Institute prostatectomy, a technique of robotic radical prostatectomy for management of localized carcinoma of the prostate: experience of over 1100 cases. Urol Clin North Am 2004; 31: 701-17.

38 Kim ED, Scardino PT, Hampel O, Mills NL, Wheeler TM, Nath RK. Interposition of sural nerve restores function of cavernous nerves resected during radical prostatectomy. J Urol 1999; 161: 188-92.

39 Klotz L. Intraoperative cavernous nerve stimulation during nerve sparing radical prostatectomy: how and when? Curr Opin Urol 2000; 10: 239-43.

40 Kim ED, Scardino PT, Kadmon D, Slawin K, Nath RK. Interposition sural nerve grafting during radical retropubic prostatectomy. Urology 2001; 57: 211-6.

41 Kim ED, Nath R, Kadmon D, Lipshultz LI, Miles BJ, Slawin KM, et al. Bilateral nerve graft during radical retropubic prostatectomy: 1-year follow up. J Urol 2001; 165 (6 Pt 1): 1950-6.

42 Scardino PT, Kim ED. Rationale for and results of nerve grafting during radical prostatectomy. Urology 2001; 57: 1016-9.

43 Kim ED, Nath R, Slawin KM, Kadmon D, Miles BJ, Scardino PT. Bilateral nerve grafting during radical retropubic prostatectomy: extended follow-up. Urology 2001; 58: 983-7.

44 Chang DW, Wood CG, Kroll SS, Youssef AA, Babaian RJ. Cavernous nerve reconstruction to preserve erectile function following non-nerve-sparing radical retropubic prostatectomy: a prospective study. Plast Reconstr Surg 2003; 111: 1174-81.

45 Anastasiadis AG, Benson MC, Rosenwasser MP, Salomon L, El-Rashidy H, Ghafar M, et al. Cavernous nerve graft reconstruction during radical prostatectomy or radical cystectomy: safe and technically feasible. Prostate Cancer Prostatic Dis 2003; 6: 56-60.

46 Walsh PC, Donker PJ. Impotence following radical prosta- tectomy: insight into etiology and prevention. J Urol 1982; 128: 492-7.

47 Lepor H, Gregerman M, Crosby R, Mostofi FK, Walsh PC. Precise localization of the autonomic nerves from the pelvic plexus to the corpora cavernosa: a detailed anatomical study of the adult male pelvis. J Urol 1985; 133: 207-12.

48 Lue TF, Zeineh SJ, Schmidt RA, Tanagho EA. Neuroanatomy of penile erection: its relevance to iatrogenic impotence. J Urol 1984; 131: 273-80.

49 Takenaka A, Murakami G, Soga H, Han SH, Arai Y, Fujisawa M. Anatomical analysis of the neurovascular bundle supplying penile cavernous tissue to ensure a reliable nerve graft after radical prostatectomy. J Urol 2004; 172: 1032-5.

50 Costello AJ, Brooks M, Cole OJ. Anatomical studies of the neurovascular bundle and cavernosal nerves. BJU Int 2004; 94: 1071-6.

51 Hollabaugh RS, Steiner MS, Dmochowski RR. Neuroanatomy of the female continence complex: clinical implications. Urology 2001; 57: 382-8.

52 Akman Y, Liu W, Li YW, Baskin LS. Penile anatomy under the pubic arch: reconstructive implications. J Urol 2001; 166: 225-30.

53 Strasser H, Bartsch G. Anatomy and innervation of the rhabdosphincter of the male urethra. Semin Urol Oncol 2000; 18: 2-8.

54 Shafik A, Doss S. Surgical anatomy of the somatic terminal innervation to the anal and urethral sphincters: role in anal and urethral surgery. J Urol 1999; 161: 85-9.

55 Benoit G, Droupy S, Quillard J, Paradis V, Giuliano F. Supra and infralevator neurovascular pathways to the penile corpora cavernosa. J Anat 1999; 195: 605-15.

56 Hollabaugh RS Jr, Dmochowski RR, Steiner MS. Neuroanatomy of the male rhabdosphincter. Urology 1997; 49: 426-34.

57 Yucel S, Baskin LS. Identification of communicating branches among the dorsal, perineal and cavernous nerves of the penis. J Urol 2003; 170: 153-8.

58 Yucel S, Baskin LS. Neuroanatomy of the male urethra and perineum. BJU Int 2003; 92: 624-30.

59 Yucel S, Baskin LS. An anatomical description of the male and female urethral sphincter complex. J Urol 2004; 171: 1890-7.

60 Yucel S, De Souza A Jr, Baskin LS. Neuroanatomy of the human female lower urogenital tract. J Urol 2004; 172: 191-5.

61 Bhandar A, Tewari A, Hemal AK, Kaul A, Badani K, Peabody JO, Menon M. Veil of Aphrodite: Definition, Scientific Foundations and Technique. 22nd World Congress on Endourology and SWL November 2-5, 2004, Mumbai, India.

62 Takenaka A, Murakami G, Matsubara A, Han SH, Fujisawa M. Variation in course of cavernous nerve with special reference to details of topographic relationships near prostatic apex: histologic study using male cadavers. Urology 2005; 65: 136-42.

63 Yucel S, Baskin LS. Neuroanatomy of the ureterovesical junction: clinical implications. J Urol 2003; 170: 945-8.

64 Baader B, Herrmann M. Topography of the pelvic autonomic nervous system and its potential impact on surgical intervention in the pelvis. Clin Anat 2003; 16: 119-30.

65 Tewari A, Peabody JO, Fischer M, Sarle A, Vallencien G, Delmas V, et al. An operative and anatomic study to help in nerve sparing during laparoscopic and robotic radical prostatectomy. Eur Urol 2003; 43: 444-54.

66 Gill IS, Ukimura O, Rubinstein M, Finelli A, Moinzadeh A, Singh D, et al. Lateral pedicle control during laparoscopic radical prostatectomy: refined technique. Urology 2005; 65: 23-7.

67 Walsh PC. Radical retropubic prostatectomy with reduced morbidity: an anatomic approach. NCI Monogr 1988: 133-7.

68 Walsh PC. Anatomic radical prostatectomy: evolution of the surgical technique. J Urol 1998; 160 (6 Pt 2): 2418-24.

69 Barocas DA, Han M, Epstein JI, Chan DY, Trock BJ, Trock BJ, et al. Does capsular incision at radical retropubic prostatectomy affect disease-free survival in otherwise organ-confined prostate cancer? Urology 2001; 58: 746-51.

70 Leissner J, Allhoff EP, Wolff W, feja C, Hockel M, Black P, et al. The pelvic plexus and antireflux surgery: topographical findings and clinical consequences. J Urol 2001; 165: 1652-5.

71 Ong AM, Su LM, Varkarakis I, Inagaki T, Link RE, Bhayani SB, et al. Nerve sparing radical prostatectomy: effects of hemostatic energy sources on the recovery of cavernous nerve function in a canine model. J Urol 2004; 172 (4 Pt 1): 1318-22.

72 Guillonneau B, Vallancien G. Laparoscopic radical prosta-tectomy: the Montsouris technique. J Urol 2000; 163: 1643-9.

73 da Silva GM, Zmora O, Borjesson L, Mizhari N, Daniel N, Khandawala F, et al. The efficacy of a nerve stimulator (CaverMap) to enhance autonomic nerve identification and confirm nerve preservation during total mesorectal excision. Dis Colon Rectum 2004; 47: 2032-8.

74 Klotz L. Cavernosal nerve mapping: current data and applications. BJU Int 2004; 93: 9-13.

75 Hanna NN, Guillem J, Dosoretz A, Steckelman E, Minsky BD, Cohen AM. Intraoperative parasympathetic nerve stimulation with tumescence monitoring during total mesorectal excision for rectal cancer. J Am Coll Surg 2002; 195: 506-12.

76 Kim HL, Mhoon DA, Brendler CB. Does the CaverMap device help preserve potency? Curr Urol Rep 2001; 2: 214-7.

77 Canto EI, Nath RK, Slawin KM. Cavermap-assisted sural nerve interposition graft during radical prostatectomy. Urol Clin North Am 2001; 28: 839-48.

78 Walsh PC, Marschke P, Catalona WJ, Lepor H, Martin S, Myers RP, et al. Efficacy of first-generation Cavermap to verify location and function of cavernous nerves during radical prostatectomy: a multi-institutional evaluation by experienced surgeons. Urology 2001; 57: 491-4.

79 Holzbeierlein J, Peterson M, Smith JJ. Variability of results of cavernous nerve stimulation during radical prostatectomy. J Urol 2001; 165: 108-10.

80 Klotz L, Heaton J, Jewett M, Chin J, Fleshner N, Goldenberg L, et al. A randomized phase 3 study of intraoperative cavernous nerve stimulation with penile tumescence monitoring to improve nerve sparing during radical prostatectomy. J Urol 2000; 164: 1573-8.

81 Kim HL, Stoffel DS, Mhoon DA, Brendler CB. A positive caver map response poorly predicts recovery of potency after radical prostatectomy. Urology 2000; 56: 561-4.

82 Klotz L. Neurostimulation during radical prostatectomy: improving nerve-sparing techniques. Semin Urol Oncol 2000; 18: 46-50.

83 O'Donnell PD, Finan BF. Continence following nerve-spar ing radical prostatectomy. J Urol 1989; 142: 1227-8.

84 Eastham JA, Kattan MW, Rogers E, Goad JR, Ohori M, Boone TB, et al. Risk factors for urinary incontinence after radical prostatectomy. J Urol 1996; 156: 1707-13.

85 Wei JT, Dunn RL, Marcovich R, Montie JE, Sanda MG. Prospective assessment of patient reported urinary continence after radical prostatectomy. J Urol 2000; 164 (3 Pt 1): 744-8.

86 Terada N, Arai Y, Kurokawa K, Ohara H, Ichioka K, Matui Y, et al. Intraoperative electrical stimulation of cavernous nerves with monitoring of intracorporeal pressure to confirm nerve sparing during radical prostatectomy: Early clinical results. Int J Urol 2003; 10: 251-6.

87 Pontes JE, Huben R, Wolf R. Sexual function after radical prostatectomy. Prostate 1986; 8: 123-6.