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Nerve-sparing radical hysterectomy: steps to standardize surgical technique
  1. Mustafa Zelal Muallem1,
  2. Yasser Diab2,
  3. Jalid Sehouli3 and
  4. Shingo Fujii4
  1. 1 Department of Gynecology with Center for Oncological Surgery,Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin,Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany, Berlin, Germany
  2. 2 Department of Gynecology, Portland Hospital, Portland, Victoria, Australia
  3. 3 Department of Gynecology with Center for Oncological Surgery,Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin,Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany, Berlin, Germany
  4. 4 Department of Gynecology and Obstetrics, Kyoto University, Kyoto, Japan
  1. Correspondence to Ass. Prof. Dr. Mustafa Zelal Muallem, Charite Universitatsmedizin Berlin, Campus Virchow-Klinikum, Berlin 13353, Germany; Mustafa-Zelal.Muallem{at}charite.de; Drzelal77{at}outlook.de

Abstract

Aim The primary objective of this review was to study and analyze techniques of nerve-sparing radical hysterectomy so as to be able to characterize and elucidate intricate steps for the dissection of each component of the pelvic autonomic nerve plexuses during nerve-sparing radical hysterectomy.

Methods This review was based on a five-step study design that included searching for relevant publications, selecting publications by applying inclusion and exclusion criteria, quality assessment of the identified studies, data extraction, and data synthesis.

Results There are numerous differences in the published literature concerning nerve-sparing radical hysterectomy including variations in techniques and surgical approaches. Techniques that claim to be nerve-sparing by staying above the dissection level of the hypogastric nerves do not highlight the pelvic splanchnic nerve, do not take into account the intra-operative patient position, nor the fact that the bladder branches leave the inferior hypogastric plexus in a ventrocranial direction, and the fact that inferior hypogastric plexus will be drawn cranially with the vaginal walls (if this is not recognized and isolated earlier) above the level of hypogastric nerves by drawing the uterus cranially during the operation.

Conclusions The optimal nerve-sparing radical hysterectomy technique has to be radical (type C1) and must describe surgical steps to highlight all three components of the pelvic autonomic nervous system (hypogastric nerves, pelvic splanchnic nerves, and the bladder branches of the inferior hypogastric plexus). Recognizing the pelvic splanchnic nerves in the caudal parametrium and the isolation of the bladder branches of the inferior hypogastic plexus requires meticulous preparation of the caudal part of the ventral parametrium.

  • cervical cancer
  • surgical procedures, operative
  • postoperative complications
  • surgical oncology
  • pelvic floor
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Highlights

  • Nerve-sparing techniques should be restricted to surgical techniques that dissect all three components of the pelvic autonomic nervous system.

  • A clear description of the surgical steps for dissecting all components of the pelvic autonomic nervous system is essential.

  • Recognition of pelvic nerves and key anatomical landmarks is a key requisite for meticulous parametrial dissection.

Introduction

Nerve-sparing radical hysterectomy has become increasingly common in the last few decades. This is principally due to a high rate of long-term post-operative complications involving the pelvic autonomic nervous system with conventional radical hysterectomy including bladder dysfunction, anorectal mobility disorders, and sexual dissatisfaction in cervical cancer survivors.1 However, there is an obvious prevalence of disparity in opinions concerning the technique and surgical approach despite agreement on the need to highlight the anatomical autonomic nerve structures and sparing these nerves also. There are also considerable differences in perspectives regarding the viability and surgical feasibility of the technique in the treatment of invasive cervical cancer.

The pelvic autonomic system is composed of the superior and inferior hypogastric plexuses. The inferior hypogastric plexus is found in the deep extra-peritoneal spaces adjacent to the pelvic viscera and is formed by contributions from the hypogastric nerves, pelvic splanchnic nerves, and sacral splanchnic/sympathetic trunk.2 3 Some authors have suggested that nerve-sparing radical hysterectomy has to be restricted to small tumors in early-stage cancers;4–7 however, there seems to be a basic misunderstanding about the technique and its applications. Nerve-sparing radical hysterectomy is not defined by any modification of radicality but rather by performing a radical hysterectomy with dissecting and sparing the autonomic nerve structures. Querleu et al8 in their latest review (2017) on Querleu-Morrow classification of radical hysterectomy (2008)9 place emphasis on the restriction of nerve-sparing techniques to radical hysterectomy type C adapted to International Federation of Gynecology and Obstetrics (FIGO) stage IB1 with deep stromal invasion and IB2-IIA or early IIB cervical cancers. This has not been defined arbitrarily but rather because of the fact that large tumors and/or deep infiltrated tumors will not be appropriately operated on without a total resection of the vesico-uterine and vesicovaginal ligaments and with a resection of adjusted length of vaginal vault with its surrounding paracolpium. This radical resection (type C) sacrifices the ventral part of the inferior hypogastric plexus, the bladder branches, and probably the pelvic splanchnic nerves (leading to type C2) without prior direct visualization and dissection of the bladder branches (in the lateral wall of the vagina/rectum) and the pelvic splanchnic nerves (in the caudal part of the lateral parametrium).

The primary objective of this review is to characterize, suggest and elucidate more intricate steps for each individual component of the pelvic autonomic nerve plexuses with reference to nerve-sparing radical hysterectomy. Consequently we have endeavoured to assess every technique according to a systematic methodology for elucidating the major structures of the pelvic autonomic nervous system that need to be spared in order to assure the integrity of proper post-operative bowel, bladder, and sexual function.

Search Strategy and Selection Criteria

This literature review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.10 A search of MEDLINE (Ovid), EMcBASE (Ovid), and Cochrane databases for studies published from January 1987 to December 2017 was performed using the search term 'nerve-sparing radical hysterectomy for cervical cancer' and limited to publications in the English language. The search strategy was rendered effective by cross-referencing keywords and subsequent second-stage use of the references within the articles identified in the first round. PubMed and PMC were searched for studies pertaining to the topic. Some 985 studies were identified in the initial search on recent trends and publications selected based on inclusion and exclusion criteria. Five hundred and thirty-three studies were excluded for not focusing on the female pelvic autonomic nervous system and/or radical hysterectomy. Three hundred and ninety nine studies were excluded because they did not pertain to specific manifestation, diagnostic, and treatment procedures. Thirty-three studies were excluded because they were editorials and not research publications. Six studies were excluded because they were letters to the editor. In the final selection, 14 studies were selected and coded as they were considered to be most appropriate to the present review. This literature review was based on a five-step study design that included searching for relevant publications in various available databases, selecting relevant publications by applying inclusion and exclusion criteria, quality assessment of the identified studies, data extraction, and data synthesis. The results and studies included in this review have been summarized in a descriptive and narrative manner. Quality assessment was done autonomously by two reviewers (MZM and YD) on the quality of the methodology.

Selection exclusion criteria included editorials, letters, abstracts, narrative reviews, and articles that did not describe surgical procedures. Cadaver studies were also excluded since tissue dissection on live patients differs from that on cadavers.

Results and Discussion

The techniques described in most of the studies begin with identification of the hypogastric nerves and the proximal part of the inferior hypogastric plexuses followed by further dissection in the same plane (ventrocaudal direction) in order to stay above the pelvic splanchnic nerves and bladder branches.11–13 In our surgical experience, which is in line with the Japanese research studies,1 14 15 direct visualization and dissection seems to be the only way to preserve hypogastric nerves, pelvic splanchnic nerves, and the bladder branches from the inferior hypogastric plexus. This is principally because the bladder branches leave the inferior hypogastric plexuses in a ventrocranial direction to merge with the bladder muscles (Figure 1A). Preparing and proceeding in the ventrocaudal direction without prior dissection of the bladder branches may damage these branches.

Figure 1

The topography of the pelvic autonomic nerve structures. (A) Inferior hypogastric plexus after nerve-sparing radical hysterectomy. The photograph shows how the bladder branches leave the plexus in a ventrocranial direction (dotted yellow line) and do not follow the ventrocaudal direction (dotted black line) of the hypogastric nerve. The photograph also illustrates the deep course of the pelvic splanchnic nerves (small yellow arrow, the nerves are isolated and highlighted with a red vessel loop). EIA, external iliac artery; EIV, external iliac vein; IGV, inferior gluteal vein; IIA, internal iliac artery; IIV, internal iliac vein; IVV, inferior vesical vessels; MUL, medial umbilical ligament. (B) The pelvic splanchnic nerves arising from the ventral rami of the sacral spinal nerves S2-S4 directly above the fibers of levator ani and crossing the pelvic floor from the pelvic wall in a mediocranial direction to join the inferior hypogastric plexus. (C) Medial view of the inferior hypogastric plexus after performing a nerve-sparing radical hysterctomy. Note that the cut ends of the sacrovaginal ligament (dotted line) and the tendinous arch of the pelvic fascia (arrows) are dorsal and medial from the inferior hypogastric plexus. Without direct visualization and isolation of all components of the inferior hypogastric plexus, resection of the sacrovaginal ligament and fascia pelvis visceralis (the tendinous arch of the pelvic fascia) to achieve an appropriate vaginal vault resection will destroy all these nerves. The small arrows (→) show the cut end of the tendinous arch of the pelvic fascia. The asterisk (★) shows the cut end of the uterine branches from the inferior hypogastric plexus. (all 3 photographes are original pictures from cervical cancer patients operated by the first author).

Raspagliesi et al16 have elucidated the surgical steps to highlight all three components of the autonomic pelvic nervous system (hypogastric nerves, pelvic splanchnic nerves, and the bladder branches from the inferior hypogastric plexus). Unfortunately, their description, and the figures used to illustrate the pelvic splanchnic nerves, do not match our current knowledge regarding the exact course of the pelvic splanchnic nerves (pelvic splanchnic nerves crossing the pelvic floor deeply, directly above the fibers of levator ani, from the pelvic wall in a mediocranial direction to join the inferior hypogastric plexus in a level between the vagina and rectum,3 which is shown in Figure 1B).

The authors have not highlighted the network of pelvic splanchnic nerves and hypogastric nerve (the cranial part of the inferior hypogastric plexus) giving rise to the uterine and bladder branches, but have described the nerve fibers from the hypogastric plexus running beside the lateral wall of the vagina to the bladder. Recognizing this cross from its lateral aspect and cutting the uterine branches only provides an opportunity to lateralize the inferior hypogastric plexus and its bladder branches, which is essential for resecting a tumor-adjusted vaginal vault. Raspagliesi et al have reported that preserving bladder branches restricts the level of colpectomy to 2 cm below the cervix, which could impair surgical radicality in stage IIA cases. Figure 1C illustrates the importance of direct visualization of the inferior hypogastric plexus before cutting the vaginal vault in order to be able to adjust its length according to tumor volume.

Charoenkwan et al described a simplified technique for nerve-sparing type C radical hysterectomy, whereby reviewing their surgical steps surgeons could manage the lateral parametrium as a single-tissue segment.17 18 The study failed to describe ways of identifying and isolating the pelvic splanchnic nerves. Moreover, the bladder branches were managed by retracting them downward and cutting the deep layer of vesico-uterine ligament anteromedial to the nerves. It is imperative to mention that in all the figures there is no illustration of the pelvic splanchnic nerves, inferior hypogastric plexus, or the bladder branches but only of the hypogastric nerves, and this is not sufficient to demonstrate nerve-sparing radical hysterectomy effectively.

In this context, Trimbos et al also recognized the need to highlight all three components of the pelvic autonomic system to be able to spare them, and described their experience and surgical steps, where the hypogastric nerve, inferior hypogastric plexus, pelvic splanchnic nerves, and bladder branches have been identified, though the resection of the dorsal leaf of the vesico-uterine ligament and the precise anatomy of the ventral parametrium were not detailed in their Leiden nerve-sparing radical hysterectomy.19 This group later abandoned the resection of the vesico-uterine ligament and the isolation of the pelvic splanchnic nerves, developing a new (no longer type C) technique (called a SWIFT operation),12 which is inspired by a total mesometrial resection.

Hoeckel et al11 had reported total mesometrial resection as a new nerve-sparing concept for radical hysterectomy, which was inspired by the total mesorectal excision technique pioneered by Heald (1982).20 This technique postulates that the dissection and isolation of hypogastic nerves bilaterally will be sufficient to spare the other autonomic pelvic structures by staying above the hypogastric nerves. This ignores the intra-operative patient position (lithotomy position) with the fact that the bladder branches leave the inferior hypogastric plexus in a ventrocranial direction and the fact that the inferior hypogastric plexus is drawn cranially (if it is not recognized and isolated earlier) above the level of the hypogastric nerves by drawing the uterus cranially during the surgery.

Hoeckel et al have further reported a 13% reduction in bladder-filling sensitivity, indicating injuries of the sympathetic nerves, which they had tried to isolate by means of the total mesometrial resection technique, and about 66% loss of contraction of the detrusor muscle, which indicates injuries to the pelvic splanchnic nerves or the bladder branches of the inferior hypogastric plexus in the first three post-operative months. A total of 53% of their patients had strained bladder function for approximately 1 year after total mesometrial resection. Later, Hoeckel did not claim that total mesometrial resection was a nerve-sparing radical hysterectomy.21–23

This procedure also compromises the radicality by abandoning the resection of the ventral parametrium. This compromised radicality was noticed in a very short anterior vaginal vault (median length was only 1 cm) in total mesometrial resection specimens.23

Possover et al have succeeded in identifying the pelvic splanchnic nerve in the caudal part of the cardinal ligament using the middle rectal artery as a landmark.24 They recognized that the parasympathetic nerves are located in the caudal part of the rectovaginal and vesicovaginal ligaments. Moreover, they have suggested that it would be better to preserve the lower part of the vesicovaginal and rectovaginal ligaments and determined that the resected vaginal cuff should involve no more than one-third of the vagina to guarantee preservation of the parasympathetic fibers. These findings led the authors to develop a new technique of radical hysterectomy called the laparoscopy-assisted vaginal radical hysterectomy.25 26

In the vaginal portion of this operation, the vaginal cuff is resected extra-fascial without resection of any part from the ventral parametrium (vesico-uterine or vesicovaginal ligament). The dissection of the vesicovaginal septum, together with evaluation of biopsies from this septum, helps in the intra-operative selection of patients with minimal risk of infiltration in the ventral parametrium. Unfortunately the issues with this technique are:

  1. Using the middle rectal artery as a landmark to recognize the vasculature from the neural part of the cardinal ligament is unfortunately not reliable as this artery has many variations. The middle rectal artery is described as an artery that penetrates the pelvic plexus from the lateral side along with the lateral ligament; the frequency of finding this lateral middle rectal artery ranges from 20% to 30%.27

  2. Abandoning resection of the vesico-uterine ligament and paracolpium would leave a rate of 11.6% of microscopic tumor infiltrations in the ventral parametrium.28

  3. The technique does not identify the nerves in the ventral parametrium but spares the bladder branches of the inferior hypogastric plexus by avoiding resection in the vesicovaginal ligament.

The Japanese surgeons recognized the issue of identifying and sparing the autonomic pelvic nervous system during the radical hysterectomy earlier. This is perhaps because they had applied the Okabayashi technique for radical hysterectomy,29 30 whereas the Western surgeons had used the Wertheim-Meigs technique as the standard procedure for radical hysterectomy.31 The main difference between the two techniques is that the Okabayashi technique defines very precisely the resection of the vesico-uterine ligament in its two layers to resect enough ventral parametrium and to open the access to resect enough paracolpium. This step has not been defined in the Wertheim-Meigs technique. Both techniques are not nerve-sparing in practical terms, but the principal of the Okabayashi technique has the advantage of understanding that a nerve-sparing technique has to directly visualize the autonomic nervous system in three dimensions of the parametrium.

The concept of nerve-sparing radial hysterectomy as a variation of the Okabayashi technique was established by Kobayashi.32 This is based on the concept of preservation of the pelvic splanchnic nerves and the pelvic plexus by separating the vascular and neural parts, containing the deep uterine vein during dissection of the lateral parametrium. Sakamoto and Takizawa further established the technique for systematic preservation of the pelvic autonomic nervous system, which contains the hypogastric nerve, pelvic splanchnic nerves, the pelvic plexus, and the bladder branches.33 34

Yabuki had shown that the lateral parametrium has more structures to be highlighted, in particular the neural parts of the pelvic splanchnic nerves.35–37 Although unfortunately they had emphasized the lateral parametrium as the main aspect of the parametrium in his earlier studies, Yabuki et al later tried to identify the bladder branches in the vesico-uterine ligament by developing an artificial space called 'the fourth space of Yabuki'.38 It is important to mention here that the fourth space of Yabuki is not identical to Okabayashi’s paravaginal space. Yabuki tried to identify the bladder branches in the deep layer of the vesico-uterine ligament without dissecting or highlighting its anatomy, whereas we now know that the bladder branches reside in the lateral side of the vaginal wall and not in the deep layer of vesico-uterine ligament, which has to be resected for direct visualization of these branches.

The technique of nerve-sparing surgery gained clarity only after the study of Sakuragi et al.15 In this study the authors described a comprehensive technique of nerve-sparing radical hysterectomy. Their technique could identify the bladder branches and the close relationship between the pelvic splanchnic nerve and the deep uterine vein and between the vesical veins and bladder branches of the inferior hypogastric plexus. The authors elucidated that the pelvic plexus is in close proximity to the paracolpium at the depth at which the vagina should be dissected, and if separation of the pelvic plexus from the paracolpium is insufficient then the pelvic plexus will be injured when the vagina is amputated. The Sakuragi study population had tumor stage ≥FIGO IB2 in approximately two-thirds of cases, with a median tumor size of 39 mm, and they concluded that separating the inferior hypogastric plexus from the paracolpium and selectively dissecting the uterine branch of the pelvic plexus is essential to facilitate the removal of a sufficient length of the vagina, without involving the pelvic plexus.

Two years later, Kato et al published a technique for nerve-sparing radical hysterectomy.39 Unfortunately, this technique lacked precision and did not recognize the bladder branches of the inferior hypogastric plexus. The authors utilized the middle rectal artery as a landmark for highlighting the pelvic splanchnic nerves and the inferior vesical artery as a landmark for recognizing and preserving the bladder branches of the inferior hypogastric plexus. After clarification of the vascular structures of the vesico-uterine ligament, the nerve-sparing radical hysterectomy by Fujii et al further highlights each component of the autonomic nervous system with a detailed description of the anatomy of the cranial and caudal leaf of the vesico-uterine ligament.40 This description allows for minimum blood loss during dissection of the paracervix leading to an overall reduction in post-surgical morbidity, and easy resection of any vaginal length deemed appropriate by the level of the cervical disease. It is true that after implementation of this technique the bladder needed to be drained for 9 days and the nerves did not seem to be completely preserved,41 but it was the first procedure to highlight all the components of the autonomic pelvic nervous system in a step-by-step procedure and to describe precisely the anatomy of the vesico-uterine ligament. It should be noted that all the patients had delayed bladder function and recovered their urinary function completely by the 21st post-operative day with this technique.1

In the next decade, the majority of publications on nerve-sparing radical hysterectomy have been comparative studies on the oncologic and functional results of the various radical hysterectomy techniques described, or on the feasibility of these techniques, or the combination of these techniques with laparoscopy, robotic surgery or other methods, without any reference to the technique used for nerve-sparing and which nerves are preserved.42 43 In our opinion this has perhaps led to discrepancies in the assessment of the nerve-sparing technique, making it more difficult to be understood and implemented.

For instance, Zahng et al have reported an improved nerve-sparing radical hysterectomy technique for cervical cancer using the paravesico-vaginal space as a new surgical landmark.44 In this context it is imperative to mention that the paravesico-vaginal space itself is not a clearly defined space and there is no precise description of the relationship between this landmark and the main components of the pelvic autonomic nervous system. Moreover, there is no specific guideline to highlight the preserved nerves. Further, the authors have reported a successful catheter removal on post-operative day 4 only in 69.4% of cases and a residual urine volume ≤50 mL in only 34.7% of patients. The most important points regarding the radicality and the clarity of nerve-sparing surgical steps in each technique are summerized in Table 1.

Table 1

The most important points regarding the radicality and the clarity of nerve-sparing surgical steps for each technique

Conclusions

This review has highlighted numerous differences in the literature regarding nerve-sparing radial hysterectomy. These include variations in the techniques and surgical approaches. Nerve-sparing radical hysterectomy does not imply any modification of radicality but performing a type C(1) radical hysterectomy with dissecting while at the same time sparing the autonomic nerve structures. It is important to emphasize that use of the term 'nerve-sparing technique' should be restricted only to surgical techniques that include a clear description of the surgical steps required to dissect all three components of the pelvic autonomic nervous system.

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Footnotes

  • Correction notice Since this aricle was first published online first, changes to affiliation 2 have been made.

  • Contributors The work was written by MZM and the other co-authors contributed to the revising, refining, and rewriting processes, and by adding comments and clarifying the purpose of the outlined technique compared with the published literature.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • Competing interests None declared.

  • Patient consent for publication Not required.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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