Anatomic identification and functional outcomes of the nerve sparing Okabayashi radical hysterectomy
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1 Gynecologic Oncology 107 (2007) Anatomic identification and functional outcomes of the nerve sparing Okabayashi radical hysterectomy Shingo Fujii, Kenji Takakura, Noriomi Matsumura, Toshihiro Higuchi, Shigeo Yura, Masaki Mandai, Tsukasa Baba, Shinya Yoshioka Department of Gynecology and Obstetrics, Postgraduate School of Medicine, Kyoto University, Sakyoku, Kyoto, , Japan Received 27 June 2007 Abstract Objectives. To clarify the anatomy necessary for the nerve sparing Okabayashi's radical hysterectomy, we meticulously separated the blood vessels and connective tissues to preserve the pelvic splanchnic nerve, the hypogastric nerve, and the bladder branch of the inferior hypogastric plexus under magnification ( 2.5) during the Okabayashi radical hysterectomy. Methods. Twenty-four patients (FIGO stage IB, n = 22, and stage IIA, n = 2) underwent meticulous nerve sparing radical hysterectomy during 2004 to Postoperative assessment of bladder function consisted of the time to (a) achieve a postvoid residual urine volume (PVR) less than 50 ml, (b) obtain a sensation of bladder fullness, and (c) obtain satisfaction of micturition. Results. Isolation of the deep uterine vein could preserve one of the branches of the pelvic splanchnic nerve. The hypogastric nerve in the lateral rectal wall was isolated to the inferior hypogastric plexus. During the division of the posterior leaf of the vesicouterine ligament (VUL), isolation of the inferior vesical vein could reveal the bladder branch from the inferior hypogastric plexus. Only the uterine branch from the inferior hypogastric plexus was isolated and divided. Then, the T-shaped nerve plane consisting of the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch from the inferior hypogastric plexus is preserved. Urinary functions: (a) 11 out of 24 patients had measured PVR of less than 50 ml by postoperative day (POD) 14 and all patients had achieved this by day 21 (mean POD: 14.64±2.04). (b) Twenty-two out of 24 patients reported a sensation of bladder fullness by POD 14 and all by POD 21 (mean POD: 11.25±1.78). (c) Seventeen out of 24 patients reported satisfaction of micturition by POD 14 and all by POD 21 (mean POD: 12.34±2.32). Conclusion. In order to accomplish the nerve sparing Okabayashi's radical hysterectomy, it is necessary to meticulously divide the posterior leaf of the vesicouterine ligament. By the separation of the inferior vesical vein in the posterior leaf of the vesicouterine ligament, the bladder branch from the inferior hypogastric plexus can be identified and preserved. All patients recovered their urinary function completely by POD Elsevier Inc. All rights reserved. Introduction The standard procedure of radical hysterectomy in Japan is based on Okabayashi's radical hysterectomy reported from Kyoto Imperial University in 1921 [1] which is characterized by the wide extirpation of the parametrial tissue and the separation of the posterior leaf of the vesicouterine ligament [1,2]. The technique enabled the surgeon to separate the bladder with the ureter completely away from the lateral side of the cervix and the vagina. With further separation of the bladder and the rectum from the vagina, the uterus with the vagina is only connected by the lateral paravaginal tissue (paracolpium). This Corresponding author. Fax: address: sfu@kuhp.kyoto-u.ac.jp (S. Fujii). dissection allows easy resection of any vaginal length deemed appropriate by the level of cervical disease. This dissection technique allowed optimization of the radical hysterectomy. However, this operation had been often associated with severe bladder dysfunction and colorectal motility disorders. Okabayashi himself in 1944 (in Japanese) proclaimed that the preservation of nerve function would be one of the challenges for future optimization of the radical hysterectomy [3]. The uterus, vagina, urinary bladder and rectum are innervated by a motor and sensory autonomic nerve supply, both of sympathetic and parasympathetic origin. The sympathetic fibers come from T11-L2 which form the superior hypogastric plexus. The parasympathetic fibers come from S2, 3 and 4 at the pelvic wall as the pelvic splanchnic nerve. These fibers merge and form the inferior hypogastric plexus which /$ - see front matter 2007 Elsevier Inc. All rights reserved. doi: /j.ygyno
2 S. Fujii et al. / Gynecologic Oncology 107 (2007) branch to innvervate the uterus and the urinary bladder [4]. Therefore, Japanese doctors have tried to preserve these nerves during radical hysterectomy in order to minimize subsequent sympathetic and parasympathetic dysfunction. Kobayashi at Tokyo University enthusiastically modified Okabayashi's method and in 1961 described the basic concept for the improving postoperative bladder function [5]. This concept was based on the preservation of the pelvic splanchnic nerve by the separation of the vascular part (containing the deep uterine vein) from the lower hard bundle (containing the splanchnic nerve) during the division of the parametrial tissues [5]. Then in 1983, Fujiwara at Kitano Hospital illustrated the importance of the preservation of the bladder branch from the inferior hypogastric plexus as well as from the pelvic splanchnic nerve defining the point of transection of the uterine branch of the pelvic nerves [6]. A similar concept was reported in 1992 in the introduction paper of the so-called Tokyo method [7]. These methods evolved to improve postoperative bladder function. However, the precise anatomy of this region to define the necessary technique to preserve the bladder branch from the inferior hypogastric plexus still remains to be elucidated. This prompted many recent analyses of the anatomy of the pelvic nerve plexus utilizing fresh cadavers [8,9,10] and the anatomic principles were then applied to the radical hysterectomy as published in the recent articles by several Japanese gynecologists such as Yabuki et al. [8,9], Kato et al. [11], Sakuragi et al. [12, 13] and Kitahara et al. [14]. Sakuragi et al. [12,13] recently reported how to identify the bladder branch from the inferior hypogastric plexus during radical hysterectomy and how to isolate and transect the uterine branch from the inferior hypogastric plexus. Moreover, recently, there are several publications addressing the preservation of pelvic nerve function from both Western and Eastern countries [10,15,16,17,18]. Through this literature, we can learn the concept of how to preserve the pelvic nerves. However, the literature lacks critical photos and/or illustrations that are necessary for us to understand the precise anatomy needed for the preservation of the bladder branch from the inferior hypogastric plexus. Therefore, there is a need for continued identification of the precise anatomical information directing the technique for optimal preservation of bladder function at the time of radical hysterectomy. It has been reported that during radical hysterectomy the hypogastric nerve is often sacrificed when the surgeon divides the uterosacral ligament and rectovaginal ligament, the pelvic splanchnic nerve when the surgeon divides the deep uterine vein in the cardinal ligament, and the bladder branch of the pelvic nerves when the surgeon ligates and divides the paracolpium (Fig. 1) [2]. Our group has recently described the precise anatomy of the vesicouterine ligament by separating the individual blood vessels which identified two major veins in the posterior leaf of the vesicouterine ligament: the middle vesical vein and the inferior vesical vein under magnification ( 2.5) during the Okabayashi's radical hysterectomy [19]. As well from 2004 to 2006, we performed nerve sparing Okabayashi's radical hysterectomy under magnification ( 2.5). In this paper, we describe the anatomy of the inferior hypogastric plexus Fig. 1. Surgical procedures that can damage the pelvic nerves. During radical hysterectomy, the hypogastric nerve is frequently injured or transected when the surgeon divides the uterosacral ligament and rectovaginal ligament (1), the pelvic splanchnic nerve when the surgeon divides the deep uterine vein in the cardinal ligament (2), the bladder branch from the inferior hypogastric plexus when the surgeon ligates and divides the vaginal blood vessels (paracolpium) (3). encompassing the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch/the uterine branch from the inferior hypogastric plexus. We describe and illustrate the procedure to identify these nerves and how to transect only the uterine branch from the inferior hypogastric plexus in order to preserve the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch from the inferior hypogastric plexus. We also report the functional outcomes from the successful completion of this procedure. Methods Women diagnosed with early stage invasive cervical cancer deemed operable between October 2004 and July 2006 were eligible. A standardized surgical approach was performed by one of the authors (SF). During Okabayashi's radical hysterectomy, individual blood vessels and nerve bundles were meticulously identified and separated under 2.5 magnification. Twentyfour patients (FIGO stage IB, n=22; and stage IIA, n=2) (TNM nomenclature: pt1b: 21, pt2a:2 and pt2b:1) underwent satisfactory meticulous nerve sparing radical hysterectomy. Mean patient age was 50.6 (range 24 72), mean body mass index (BMI) was 21.0 (range ) and mean tumor diameter was 3.15 cm (range cm). All patients had an indwelling Foley catheter for 9 days that was standard practice for all patients who underwent a conventional Okabayashi's radical hysterectomy. Therefore, we applied the same period of catheterization for the nerve sparing Okabayashi's radical hysterectomy. Postoperative assessment of bladder function was begun on postoperative day 10. Voiding trials were performed every 4 h and the postvoid residual urine volume (PVR) was measured by catheterization. The primary endpoint for bladder function was the time to achieve a PVR less than 50 ml. Secondary endpoints of bladder function were measured by patient self-report of (a) the time to obtain a sensation of bladder fullness, and (b) the time to achieve satisfaction of micturition were compared to those of the sensations before the surgery. Operative procedure Only the operative steps that are necessary to elucidate the anatomy of the pelvic nerves.
3 6 S. Fujii et al. / Gynecologic Oncology 107 (2007) 4 13 Fig. 2. (A) Separation and isolation of the deep uterine vein in the parametrium. (B) Illustration of the deep uterine vein in the parametrium. Isolation and separation of the deep uterine vein from the pelvic splanchnic nerve After pelvic lymphadenectomy, the uterine artery is transected close to the internal iliac artery. Then, the pararectal and the paravesical spaces are developed. Between the two spaces, we can appreciate a thick bundle of parametrial connective tissue, in which the superficial uterine vein and the inferior vesical artery (not always) are carefully isolated, clamped, cut and ligated. Then we isolated, clamped, cut and ligated the deep uterine vein (Figs. 2A, B). Beneath the deep uterine vein, we can usually appreciate one of the branches of the pelvic splanchnic nerves (Figs. 3A, B) that runs toward the inferior hypogastric plexus. Isolation and separation of the hypogastric nerve On the rectal side of the pararectal space, the hypogastric nerve running parallel with the rectum is isolated (Figs. 4A, B) and a vessel tape is applied as a marker. The peritoneum of the pouch of Douglas and posterior peritoneal leaves of the broad ligament are transversely incised. The connective tissue on the vaginal wall is separated from the central wall of the rectum deep enough to permit extirpation of an ample vaginal cuff. Division of the uterosacral ligament By the separation of the vaginal wall from the rectum and, thereafter, pushing the rectum up, the uterosacral ligament visible between the lateral sidewall of the uterus and the rectum is divided not including the hypogastric nerve. Separation of the cut end of the deep uterine vein from the pelvic splanchnic nerve The cut end of the deep uterine vein is separated from the connective tissues of the rectal lateral sidewall, that includes the branch of the splanchnic nerve, down to the level of the inferior hypogastric plexus. Separation of blood vessels in the posterior leaf of the vesicouterine ligament Following the meticulous separation of the anterior leaf of the vesicouterine ligament as described in our previous paper [19], the connective tissue in the posterior leaf of the vesicouterine ligament is carefully separated and the middle vesical vein, that runs from the urinary bladder to the cervix draining into the deep uterine vein (Figs. 5A, B), is doubly clamped, divided and ligated. Fig. 3. (A) Division of the deep uterine vein reveals the pelvic splanchnic nerve. (B) Illustration of the pelvic splanchnic nerve beneath the deep uterine vein.
4 S. Fujii et al. / Gynecologic Oncology 107 (2007) Fig. 4. (A) Separation of the hypogastric nerve from the sidewall of the rectum in the pararectal space. (B) Illustration of the hypogastric nerve. Isolation and division of the inferior vesical vein In addition, we can appreciate a vein (inferior vesical vein) that runs parallel to the cervix from the posterior portion of the urinary bladder, which also drains into the deep uterine vein (Figs. 6A, B). If we trace the splanchnic nerve and the hypogastric nerve toward the inferior hypogastric plexus and to the urinary bladder, definite nerve bundles running from the plexus to the bladder beneath the inferior vesical vein are visualized (Figs. 6A, B). When the inferior vesical vein is easily isolated, the vein is doubly clamped, ligated and divided. Then, the bladder branch from the inferior hypogastric plexus running parallel with the blood vessels of the paracolpium becomes clear. If it is difficult to isolate the inferior vesical vein, it is possible to clamp the vein with the paravaginal blood vessels at the time of the division of the paracolpium. Separation/division of the uterine branch from the inferior hypogastric plexus By tracing the hypogastric nerve toward the posterior-lateral wall of the uterus, we appreciate the inferior hypogastric plexus formed by the hypogastric nerve, the splanchnic nerve, the bladder branch and the uterine branch from the inferior hypogastric plexus (Figs. 7A, B). These nerves reside in the same connective tissue plane that we call the pelvic nerve plane. Then Pean's forceps is insinuated from the v-shaped depression created between the bladder branch and the blood vessels of the paracolpium into the connective tissue between the pelvic nerve plane and the cervix/upper vagina at the level a little bit ventral side of the hypogastric nerve (Figs. 7A, B and 8A, B). The uterine side of the pelvic nerve plane including the uterine branch from the inferior hypogastric plexus is doubly clamped, divided, and ligated. When we cut the uterine branch of the pelvic nerves, there is a feeling resembling a stretched string breaking with a snap and the pelvic side of the nerves such as the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch of the inferior hypogastric plexus forms the T-shaped nerve plane (Figs. 9A, B). By pushing the rectum up, the rectovaginal ligament rises to the surface between the pelvic nerve plane and the rectum. Only the rectovaginal ligament is divided using bipolar scissors toward the upper vagina excluding the pelvic nerve plane. Separation and division of the paracolpium If we divide the remaining rectovaginal ligament close to the upper vagina, the bladder branch from the inferior hypogastric plexus is gradually separated from the blood vessels of the paracolpium. The separation can extend caudally to obtain vaginal length deemed appropriate by the level of cervical disease. At the designated level, the blood vessels of the paracolpium are doubly clamped (Figs. 10A, B), cut and ligated (Figs. 11A, B). Then the T-shaped nerve plane formed Fig. 5. (A) Separation of the middle vesical vein in the posterior leaf of the vesicouterine ligament. (B) Illustration of the middle vesical vein.
5 8 S. Fujii et al. / Gynecologic Oncology 107 (2007) 4 13 Fig. 6. (A) Isolation of the inferior vesical vein reveals the bladder branch from the inferior hypogastric plexus. (B) Illustration of the relationship between the inferior vesical vein and the bladder branch from the inferior hypogastric plexus. by the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch of the inferior hypogastric nerve is completely preserved (Figs. 11A, B). By dividing the paracolpium, the uterus is only connected with the vagina. After the same procedure on the opposite side, the length of the vaginal cuff is confirmed. Then the whole vagina is clamped with a right angle forceps and the uterus is amputated from the vagina. The view of the T-shaped nerve plane after the removal of the uterus The T-shaped nerve plane including the bladder branch of the pelvic nerves after the removal of the uterus is demonstrated (Fig. 12). Results Urinary function Postoperative assessment of bladder function was objectively measured by assessing the time to obtain a postvoid residual urine volume (PVR) of 50 ml. Subjective measures of self-reported sensation of bladder fullness and satisfaction of micturition were evaluated after draining the bladder for 9 days using Foley catheter. The time to achieve a PVR 50 ml The shortest time to achieve a PVR 50 ml was within 2 days and the longest was 10 days after removal of Foley catheter (Tables 1 and 2). If we assess the period of PVR as postoperative days (POD), 11 out of 24 patients achieved the desired PVR by POD 14 (5 days after removal of the foley catheter) and all patients achieved the target PVR by POD 21. The mean time to reach the target PVR was POD 14.64±2.04. The period to obtain a sensation of bladder fullness Patients reported a sensation of bladder fullness sooner than demonstrating the desired PVR (Tables 1 and 2). Some patients reported immediate sensation of bladder fullness and the longest Fig. 7. (A) Separation of the hypogastric nerve, the pelvic splanchnic nerve and the bladder branch clearly reveals the inferior hypogastric plexus and the uterine branch from the plexus. These nerves comprise a plane that we call the pelvic nerve plane. (B) Illustration of the inferior hypogastric plexus.
6 S. Fujii et al. / Gynecologic Oncology 107 (2007) Fig. 8. (A) Separation of the uterine branch from the inferior hypogastric plexus. (B) Illustration of the separation of the uterine branch from the inferior hypogastric plexus. time to perceive this sensation was 7 days after removal of Foley catheter. The majority of patients, 22 out of 24 patients (92%) reported a sensation of bladder fullness by POD 14 and all patients could obtain a sensation of bladder fullness by POD 21. The mean time to achieve a sensation of bladder fullness was POD 11.25±1.78. Self-reported satisfaction of micturition The time to obtain satisfaction of micturition was shorter than the time to achieve a PVR 50 ml but longer than the time to obtain a sensation of bladder fullness (Tables 1 and 2). The shortest reported time was immediate and the longest was 7 days after removal of the Foley catheter. Seventeen of the 24 patients (71%) reported satisfactory micturition by POD 14 and all patients reported satisfaction of micturition by POD 21. The mean time to obtain satisfactory micturition was POD ±2.32. Discussion This study demonstrates that by the meticulous separation and division of blood vessels in the parametrium, particularly the deep uterine vein, we can preserve one of the branches of the pelvic splanchnic nerve that runs beneath the deep uterine vein toward the inferior hypogastric plexus as primarily described by Kobayashi [5]. If each blood vessel in the parametrial tissues is not isolated, there is a high probability of damage to one of the branches of the pelvic splanchnic nerve. Indeed, in order to remove the parametrium as widely as possible and optimize surgical cure, the original Okabayashi radical hysterectomy did not attempt preservation of the branches of the pelvic splanchnic nerve [1,2]. By applying traction on the cut end of the deep uterine vein, the uterine side of the deep uterine vein is separated from the pelvic splanchnic nerve. Usually this procedure does not accompany any bleeding, but there may Fig. 9. (A) Division of the uterine branch from the inferior hypogastric plexus. The T-shaped nerve plane is appreciated. (B) Illustration of the division of the uterine branch from the inferior hypogastric plexus.
7 10 S. Fujii et al. / Gynecologic Oncology 107 (2007) 4 13 Fig. 10. (A) Clamping the blood vessels of the paracolpium. The bladder branch from the inferior hypogastric nerve is clearly separated from the paracolpium. (B) Illustration of the relationship between the paracolpium and the bladder branch from the inferior hypogastric plexus. be a small blood vessel running along the pelvic splanchnic nerve. In this case, the small blood vessel becomes necessary to clamp, divide and ligate. The hypogastric nerve is then identified as the white nerve fibers within the connective tissue of the lateral rectal wall that has continuity with the connective tissue surrounding the ureter. After confirmation of the hypogastric nerve, the uterosacral ligament is divided meticulously excluding the hypogastric nerve. If we divide the uterosacral ligament without confirmation of the hypogastric nerve, the hypogastric nerve will likely be injured or cut during the division of the uterosacral ligament as previously described [12,15,16]. Indeed, in order to remove the most lateral aspects of the parametrium, Okabayashi developed the pararectal space from the point closest to the lateral side of the rectal wall after the division of the uterosacral ligament. Therefore, the hypogastric nerve was always divided at the time of this wide development of the pararectal space [1,2]. After division of the anterior leaf of the vesicouterine ligament, the posterior leaf of the vesicouterine ligament is separated as described in our previous report [19]. In the posterior leaf of the vesicouterine ligament, one usually appreciates the middle vesical vein that runs from the urinary bladder and drains into the deep uterine vein. After division of the middle vesical vein, we usually isolate the inferior vesical vein that also runs from the urinary bladder and drains into the deep uterine vein. Beneath the inferior vesical vein, the nerve bundle that runs from the pelvic splanchnic nerve toward the urinary bladder is identified. This is the bladder branch that also has a connection with the inferior hypogastric plexus. In order to identify the bladder branch from the inferior hypogastric plexus, it is better to remove the fat tissues residing between the Fig. 11. (A) Division of the paracolpium and the preservation of the uterine branch from the inferior hypogastric plexus. (B) Illustration of the division of the paracolpium and the preservation of the uterine branch from the inferior hypogastric plexus.
8 S. Fujii et al. / Gynecologic Oncology 107 (2007) Table 2 Bladder function of the 24 cases The period of PVR to become less than 50 ml was assessed The period to obtain a sensation of bladder fullness The period to obtain satisfaction of micturition POD: % (11/24) 91.7% (22/24) 70.8% (17/24) POD:21 100% (24/24) 100% (24/24) 100% (24/24) Average (days) 14.64± ± ±2.32 PVR: postvoid residual urine volume; POD: postoperative day. Fig. 12. Illustration of the T-shaped nerve plane after the removal of the uterus. dorsal portion of the urinary bladder and the rectal sidewall where one of the branches of the pelvic splanchnic nerve is running up from the pelvic floor. By this procedure, the branch of the pelvic splanchnic nerve becomes more visible and the inferior hypogastric plexus formed by the merger of the hypogastric nerve, pelvic splanchnic nerve and the bladder branch/the uterine branch of from the inferior hypogastric plexus which exhibits the shape of cross. All these nerves are included in the same connective tissue plane that is able to be separated from the lateral wall of the lower cervix/the upper vagina and the rectum. We call this plane the pelvic nerve plane. Table 1 Age, BMI, TNM nomenclature and postoperative day for the recovery of the each urinary function Name Age KMI TKM PVR less than 50 ml Sensation of bladder fullness WN pt1b TY pt1b WM pt1b HS pt1b TO pt1b KI pt1b WF PT2a YI pt1b IY pt1b IT PT2a TS pt1b SH PT2a WK PT1b KY pt1b KN PT2a HK FT1b KM FT1b NT pt1b TM pt1b IT pt1b TT PT2b HK pt1b KT pt1b KK pt1b Satisfaction of micturition Immediately above the level of the inferior hypogastric plexus, we isolate and divide the uterine branch from the inferior hypogastric plexus. After the division of the uterine branch, the bladder branch is separated from the blood vessels of the paracolpium. Only the blood vessels of the paracolpium are divided. Then the bladder branch from the inferior hypogastric plexus is clearly preserved with the pelvic splanchnic nerve and the hypogastric nerve which form the T-shaped nerve plane. If we clamp the paracolpium in a lump without recognition and separation of the bladder branch of the pelvic nerves, there is high possibility of injury to the bladder branch of the pelvic nerves. The biggest difference of the original Okabayashi's radical hysterectomy [1,2] and this reported nerve sparing Okabayashi's radical hysterectomy is in the division versus preservation of the pelvic nerve plane. The original Okabayashi method divided the pelvic nerve plane which was removed with the tumor specimen. However, the nerve sparing Okabayashi's radical hysterectomy is modified to preserve the whole pelvic nerve plane except for the uterine branch from the inferior hypogastric plexus without compromising the lateral extent of the parametrial margin. The goal of this nerve sparing procedure is to optimize postoperative bladder function as close to preoperative function as possible. Our postoperative assessment questionnaire was issued daily and included three key questions aimed at subjective assessment of postoperative: (1) Do you feel a sense of bladder fullness? (2)Can you void urine completely? (3) Do you feel satisfaction at the time of micturition? We hypothesized that meticulous identification of the surgical anatomy and preservation of the bladder branch from the inferior hypogastric plexus would result in earlier and more complete recovery of urinary function near that felt before surgery. In this study, urinary function after the nerve sparing surgery was satisfactory for almost all patients, because they could achieve a sensation of bladder fullness, satisfaction of micturition and minimal PVR within 21 days after the surgery or 12 days after removal of the Foley catheter. The shortest time to achieve the target PVR was 2 days and the longest was 10 days after the removal of Foley catheter. Bladder fullness was the first function to quickly return followed by self-reported satisfaction of micturition. This suggests that the sympathetic function is better preserved than the parasympathetic function. The reason for this difference is unclear. However, in our operative procedure, an adverse effect of the heat of the bipolar
9 12 S. Fujii et al. / Gynecologic Oncology 107 (2007) 4 13 scissors during the separation of deep uterine vein from the pelvic splanchnic nerve might have a greater effect on the recovery of the parasympathetic nerve function. Historically, patients who underwent the original Okabayashi's radical hysterectomy without nerve preservation can void and ultimately achieve a PVR less than 50 ml usually by POD 21 to 30, but the voiding pattern is usually different. Ninety-five percent of patients have to void using abdominal muscular pressure and report a loss of the sensation of bladder fullness without the satisfaction of micturition. And 5% of patients have to void by self-catheterization. Therefore, in order to obtain the urinary function with sensations of bladder fullness and satisfaction of micturition after the surgery, this kind of meticulous nerve preserving surgery is necessary. Comparison of the urinary function of our patients to the previous reports of nerve sparing radical hysterectomy is difficult because the extent of radical hysterectomy and the evaluation of the urinary function of each study are a little bit different. In the procedure of radical hysterectomy, the resection landmarks of the parametrium differ between Western countries and Japan. In the Western countries, the lines of resection of the radical hysterectomy are defined according to the classification of Piver, Rutledge, and Smith [20]. According to this classification, Class III (Meigs) radical hysterectomy is described as the dissection of the ureter from the pubovesicle ligament is complete to entry into the bladder except that a small lateral portion of the pubovesicle ligament between the lower end of the ureter and the superior vesicle artery is preserved, thus maintaining some blood supply to the distal ureter. For the young patient with a small invasive lesion (Stage I to IIa) a Class III operation is performed [20]. The Class IV radical hysterectomy is described as follows: the complete removal of all periureteral tissue, a more extensive excision of the perivaginal tissues [20]. The Class III radical hysterectomy has been believed to be a more radical surgery than that of the Wertheim method and almost identical to that of Okabayashi's radical hysterectomy. However, Okabayashi's method is completely different on the point of the separation and division of the posterior leaf of the vesicouterine ligament that is the complete removal of all periureter tissue [1,2,19]. It is different, but if we may classify Okabayashi's radical hystectomy into Piver et al.'s classification [20], it may be classified as Class IV radical hysterectomy. Therefore, we cannot primarily compare the data based on the Okabayashi radical hysterectomy with that of the Class III radical hysterectomy. The original Okabayashi radical hysterectomy was more radical than that of the Class III radical hysterectomy and usually the pelvic nerve plane is sacrificed as described above. As stated by Okabayashi himself, the preservation of nerve function is the challenges in the future [3]. However, as shown in this paper, in the operative procedures of Okabayashi's method, there was a way to preserve pelvic nerves. Particularly, the Okabayashi's procedure of the division of the posterior leaf of the vesicouterine ligament was essential for the detection of the bladder branch of the pelvic nerves. Meticulous operation following the concept of the Okabayashi method [19] finally showed that the separation of the inferior vesical vein in the posterior leaf of the vesicouterine ligament is very important to find the bladder branch from the inferior hypogastric plexus. In order to perform this kind of meticulous nerve sparing radical hysterectomy, it is necessary to wear loupes ( 2.5) for magnification and it takes more hours (average 340 min) than the original Okabayashi radical hysterectomy (average 210 min). However, the urinary function obtained through this nerve sparing surgery is better than that of the original method and justifies the longer operative time. With regard to the adequacy of radicality of this nerve sparing radical hysterectomy, long-term survival or time to progression is not yet known. This technique seems very feasible for patients with Stage Ib1 disease. However, this method may not be completely safe for the Stage IIb patients. As described by Sakuragi et al. [12], the cases that could preserve only one side of the pelvic nerve recovered favorable urinary function suggest a possibility of the preservation of the pelvic nerves that is not invaded by carcinoma. In conclusion, this is the first report that describes a precise network of pelvic nerve plane and by the division of only the uterine branch from the inferior hypogastric plexus we can accomplish nerve sparing Okabayashi's radical hysterectomy that can achieve timely and complete urinary function after the surgery. We have to realize here that the importance of the division of the posterior leaf of the vesicouterine ligament initiated by Hidekazu Okabayashi [1,2] is the key for the preservation of the bladder branch from the inferior hypogastric plexus. Acknowledgments We would like to acknowledge Dr. Carolyn Y. Muller, MD, Director, Gynecologic Oncology, Department of Obstetrics and Gynecology, University New Mexico, for reviewing and editing the manuscript. References [1] Okabayashi H. Radical abdominal hysterectomy for cancer of the cervix uteri, modification of the Takayama operation. Surg Gynecol Obstet 1921;33: [2] Okabayashi H. Radical operation of cervical cancer (in Japanese). Tokyo: Kanehara Pubulishing Co; [3] Okabayashi H. Comments to the article entitled Mibayashi's radical surgery for cervical cancer (in Japanese). Jpn Med Wochenschr, Tokyo 1944;1124:8 10. [4] Amussen M, Miller A. Clinical gynecological urology. London: Blackwell Scientific Publications; [5] Kobayashi T. Abdominal radical hysterectomy with pelvic lymphadenectomy for cancer of the cervix (in Japanese). Tokyo: Nanzando; [6] Fujiwara T. Surgery for Cervical Cancer (in Japanese); Igakutoshyosyuppan, Tokyo. [7] Sakamoto S. Radical hysterectomy with pelvic lymphadenectomy the Tokyo method. In: Coppleson M, editor. Gynecologic oncology. 2nd ed. Edinburgh: Churchill Livingstone; p [8] Yabuki Y, Asamoto A, Hoshiba T, Nishimoto H, Kitamura S. Dissection of the cardinal ligament in radical hysterectomy for cervical cancer with emphasis on the lateral ligament. Am J Obstet Gynecol 1991;164:7 14.
10 S. Fujii et al. / Gynecologic Oncology 107 (2007) [9] Yabuki Y, Sasaki H, Hatakeyama N, Murakami G. Discrepancies between classic anatomy and gynecologic surgery on pelvic connective tissue structure: harmonization of those concepts by collaborative cadaver dissection. Am J Obstet Gynecol 2005;193:7 15. [10] Ercoli A, Delmas V, Gadonneix P, Fanfani F, Villet R, Paparella P, Mancuso S, Scambia G. Classical and nerve-sparing radical hysterectomy: an evaluation of the risk of injury to the autonomous pelvic nerves. Surg Radiol Anat 2003;25: [11] Kato T, Murakami G, Yabuki Y. A new perspective on nerve-sparing radical hysterectomy: nerve topography and over-preservation of the cardinal ligament. Jpn J Clin Oncol 2003;33: [12] Sakuragi N, Todo Y, Kudo M, Yamamoto R, Sato T. A systematic nervesparing radical hysterectomy technique in invasive cervical cancer for preserving postsurgical bladder function. Int J Gynecol Cancer 2005;15: [13] Todo Y, Kuwabara M, Watari H, Ebina Y, Takeda M, Kudo M, Yamamoto R, Sakuragi N. Urodynamic study on postsurgical bladder function in cervical cancer treated with systematic nerve-sparing radical hysterectomy. Int J Gynecol Cancer 2006;16: [14] Katahira A, Niikura H, Kaiho Y, Nakagawa H, Kurokawa K, Arai Y, Yaegashi N. Intraoperative electrical stimulation of the pelvic splanchnic nerves during nerve-sparing radical hysterectomy. Gynecol Oncol 2005;98: [15] Trimbos JB, Maas CP, Deruiter MC, Peters AA, Kenter GG. A nervesparing radical hysterectomy: guidelines and feasibility in Western patients. Int J Gynecol Cancer 2001;11: [16] Maas CP, Trimbos JB, De Ruiter MC, van de Velde CJ, Kenter GG. Nerve sparing radical hysterectomy: latest developments and historical perspective. Crit Rev Oncol/Hematol 2003;48: [17] Raspagliesi F, Ditto A, Fontanelli R, Solima E, Hanozet F, Zanaboni F, Kusamura S. Nerve-sparing radical hysterectomy: a surgical technique for preserving the autonomic hypogastric nerve. Gynecol Oncol 2004;93: [18] Charoenkwan K, Srisomboon J, Suprasert P, Tantipalakorn C, Kietpeerakool C. Nerve-sparing class III radical hysterectomy: a modified technique to spare the pelvic autonomic nerves without compromising radicality. Int J Gynecol Cancer 2006;16: [19] Fujii S, Takakura K, Matsumura N, Higuchi T, Yura S, Mandai M, Baba T. Precise anatomy of the vesico-uterine ligament for radical hysterectomy. Gynecol Oncol 2007;104: [20] Piver MS, Rutledge F, Smith JP. Five classes of extended hysterectomy for women with cervical cancer. Obstet Gynecol 1974;44:
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