Yabuki2000

Gynecologic Oncology 77, 155–163 (2000) doi:10.1006/gyno.1999.5723, available online at http://www.idealibrary.com on

Radical Hysterectomy: An Anatomic Evaluation of Parametrial Dissection Yoshihiko Yabuki, M.D., Ph.D.,* ,1 Akihiro Asamoto, M.D., Ph.D.,* Tsutomu Hoshiba, M.D., Ph.D.,* Hideaki Nishimoto, M.D.,* Yukiko Nishikawa, M.D.,* and Takao Nakajima, M.D., Ph.D.† *Department of Obstetrics & Gynaecology, Ishikawa Prefectural Central Hospital, Kanazawa, Japan; and †Department of Urology, Ishikawa Prefectural Central Hospital, Kanazawa, Japan Received September 22, 1999

uterine ligament [2]. Further problems that still remain to be investigated are minimization of bleeding accompanying vesicouterine ligament dissection and a more anatomically defined preservation of pathways for the intrapelvic autonomic nerves.

Latzko [3, 4] and Okabayashi [5, 6] made a great contribution to surgery in designing operative procedures. They defined the pararectal and paravesical spaces in the parametria which were divided by three ligaments, with the concept of these two procedures being very similar. However, while Latzko dissected the parametrium in the order of the anterior, middle, and posterior ligaments, Okabayashi’s dissection was in the reverse order. Further, while Okabayashi dissected the anterior ligament following division of the vesicouterine ligament into the superficial and deep layers, Latzko aimed at only the superficial layer of Okabayashi when dissecting the vesicouterine ligament. In addition, the pararectal space in the Okabayashi procedure develops between the mesoureter and rectouterine ligament by opening up a space between the posterior leaf of the broad ligament and ureter. On the contrary, the pararectal space described in the Latzko procedure in Peham-Amreich’s textbook [4] develops between the mesoureter and pelvic wall by opening up the space between the internal iliac artery and ureter. From this we can see that these two operative procedures clearly differ.

The characteristics of the intrapelvic viscera are such that organs with totally different structure and function are suspended as a packed mass in a space termed the lesser pelvis.

Further, it is common knowledge that the mechanism of support and fixation for the pelvic connective tissue is divided into true musculofascial structures and areolar tissue including vessels and nerves [7].

In this study the authors attempted to fuse the concept of Latzko’s and Okabayashi’s procedures in order to decrease the amount of bleeding and to prevent the occurrence of neurogenic bladder during vesicouterine ligament dissection, in addition to constructing a new concept of surgical anatomy by means of histological, functional, and structural reclassification of the pelvic connective tissues, and establishing a new oper-

Objectives. This study was designed to demonstrate a reduction in the amount of blood loss for vesicouterine ligament dissection and to investigate the intrapelvic autonomic nerve pathway and its preservation by means of anatomic analysis.

Methods. The anchoring mechanism of the pelvic viscera to the pelvic wall was divided into a supporting system facing laterally and a suspensory system facing dorsoventrally. An operative procedure was designed in which both systems were separated and dissected independently.

Results. Between the two systems, an artificial space was developed, which required a new dissection method for the parametrium and revealed a new anatomic pathway for the ureter and autonomic nerve. The amount of blood loss (mean ⴞ SD) during dissection of the vesicouterine ligament was ultimately 260.1 ⴞ 114.8 ml. Postoperatively, the maximum capacity of the bladder was 393.9 ⴞ 40.4 ml, maximum detrusor pressure 6.3 ⴞ 4.1 cm H 2O, mean compliance >10 ml/cm H 2O, residual urine 23.8 ⴞ 9.4 ml, and maximum flow rate 25. ⴞ 8 2.2 ml/s, respectively.

Conclusion. A new classification for the parametrium and its dissection method have been established. Development of this new operative procedure has also contributed to a decrease in blood loss and preservation of bladder function. © 2000 Academic Press Key Words: radical hysterectomy; pelvic anatomy; vesicouterine ligament dissection; autonomic nerve preservation.

INTRODUCTION One of the unsolved aspects of radical hysterectomy is the absence of a clear theoretical background for preventing neurogenic bladder and excessive bleeding. Nevertheless, the problem of bleeding has largely been solved during cardinal ligament dissection by our dividing it into the transverse cervical ligament (of Mackenrodt) and lateral ligament with preservation of the latter [1]. Similarly, neurogenic bladder is virtually avoided by preservation of the lateral ligament and minimal dissection of the Okabayashi’s deep layer of vesico1 To whom reprint requests should be addressed at Department of Obstetrics and Gynaecology, Ishikawa Prefectural Central Hospital, 153 Minami-Shinbo Nu, Kanazawa, Ishikawa 920-8530, Japan. Fax: 81-76-238-2337.

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0090-8258/00 $35.00 Copyright © 2000 by Academic Press All rights of reproduction in any form reserved.

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TABLE 1 Urodynamics Values after Radical Hysterectomy

V max RU Q max P det 䡠 max

Standard value a

Planning stage

Implementation stage

⭌300 ml ⬉50 cm H 2O (⬍50 years of age) ⭌ 25 ml/s (⭌50 years of age) ⭌ 18 ml/s 0–30 cm H 2O

346.5 ⫾ 28.5 12.5 ⫾ 5.7

393.0 ⫾ 40.4 23.8 ⫾ 9.4

25.0 ⫾ 2.4 19.8 ⫾ 9.3

25.8 ⫾ 2.2 6.3 ⫾ 4.1

Note. V max, maximum cystometric capacity; RU, residual urine; Q max, maximum flow rate; P det 䡠 max, maximum detrusor pressure; P det, bladder pressureabdominal pressure. a Standard values for Japanese women [8].

ative procedure based on this anatomy. Further, these studies were carried out so that they could be applied to laparoscopic radical hysterectomy combined with a total abdominal radical hysterectomy.

FIG. 2. Schematic illustration of the supporting system. The stem of the supporting system is shown with a faint line. Only the blood vessels of the lower half of the lamina ligamenti umbilicalis lateralis and upper half of the cardinal ligament are figured. The reflected plane is shown with a horizontal line, and also the appearance of the suspensory system enveloped by the supporting system. The ureter passes through the space between the posterior leaf of the broad ligament and mesoureter, crosses with the uterine artery, and passes through the space between the superficial layer of the vesicouterine ligament and the reflected plane of the lamina ligamenti umbilicalis lateralis, finally reaching the bladder. A, bladder; B, uterus; C, rectum; D, lamina ligamenti umbilicalis lateralis; E, fascia of cardinal ligament; F, areolar tissue of cardinal ligament; G, lateral ligament; H, deep layer of vesicouterine ligament; I, reflection of lamina ligamenti umbilicalis lateralis; J, mesoureter K, uterine artery; L, deep uterine vein; M, superior vesical artery; N, superior vesical vein; O, middle rectal vessels; P, lateral umbilical ligament; Q, internal iliac vessels; R, ureter; S, superficial layer of vesicouterine ligament; T, rectouterine/vaginal ligament.

PATIENTS AND METHODS

FIG. 1. Schematic illustration of the suspensory system. Right oblique view of the frontal section of the bladder, vagina, and rectum in the plane of connecting both paravesical spaces. The parietal fascia, forming a tendinous arc of pelvic fascia, develops into a ligamentous structure, attaching to the pubis, linking the rectum, uterus, and bladder in succession. The star refers to the cross section of the pelvic wall and viscera of the supporting system. A, uterine body; B, bladder; C, uterine cervix; D, rectum; E, vesical fascia; F, uterine fascia; G, rectal fascia; H, pubovesical ligament; I, vesicouterine/ vaginal ligament; J, rectouterine/vaginal ligament K, rectosacral ligament; L, tendinous arc of the pelvic fascia; M, parietal fascia of the pelvis; N, supporting system; O, so-called sacrouterine ligament; P, broad ligament; Q, internal iliac artery; R, lateral umbilical artery and ligament.

The patients who were under anatomic study were as follows: (1) five radical hysterectomy patients for third-stage cervical cancer with combination surgery for other organs from 1990 to 1998, including partial cystectomy with ureteroneocystomy for three patients, total cystectomy for one patient, and anterior resection of the rectum for one patient; (2) five rectal cancer patients with anterior resection of the rectum accompanied with radical hysterectomy between 1985 to 1998; and (3) one patient with bladder cancer who underwent total cystectomy accompanied with radical hysterectomy. Intraoperative observation and macro/microscopic analyses of the excised tissues were done with reference to a comparison of the results from perioperative magnetic resonance imaging.

For the vesicouterine ligament dissection study, there were

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weight of gauze from separation of the bladder, through dissection of the bilateral vesicouterine ligament to completion of the operation. The effects of surgery on bladder function were examined at a point after the amount of residual urine was stable which was from 3 to 6 months postoperative. Urodynamic studies (Urolab Janus and Digital Automatic Uroflowmeter, Life Tech, Inc.) were performed on patients in the trial and implementation stages and calculations from these studies were used to determine the following maximum volume of the bladder, maximum detrusor pressure, compliance, amount of residual urine, and maximum flow rate of the urine using cystometry. The standard values for Japanese women are indicated in Table 1 [8], instead of presenting preoperative studies which were rejected by most of the patients.

Surgery by the author was carried out under a ureteric catheterization which was left for 2 or 3 days. The Foley catheter was removed after 7 to 10 days postoperatively.

All the figures are drawn on the right-hand side of the body.

FIG. 3. Four spaces created between the parametria. The four spaces that are excavated around the neurovascular stalk, and reflected plane with ureter still attached. Pathways for both the ureter and the autonomic nerve correspond approximately with each other. A, paravesical space; B, Latzko’s pararectal space; C, Okabayashi’s pararectal space; D, fourth space; E, bladder; F, uterine cervix; G, uterine body; H, fascia of cardinal ligament; I, areolar tissue of cardinal ligament; J, uterine artery; K, lateral umbilical ligament; L, internal iliac artery; M, ureter; N, superficial layer of vesicouterine ligament.

22 patients with cervical cancer (stage I, 17; and stage II, 5) and 11 with cancer of the uterine corpus (IIa, 7; and IIb, 4) who underwent surgery between January 1996 and March 1999.

The mean (⫾SD) age of these patients was 49.5 ⫾ 14.0 years.

The amount of blood loss, recovery of bladder function following surgery, and our new surgical procedure were analyzed according to the following three stages: the planning stage when only anatomic observation and traditional procedures were carried out on 10 patients from January 1996 to December 1996; for the trial stage on 10 of the patients when new vesicouterine ligament dissection was partially introduced from January 1997 to December 1997; and the implementation stage when new vesicouterine ligament dissection was fully implemented on 13 patients from January 1998 to March 1999.

Values are indicated as mean (⫾SD), and the Levene test was used to determine any statistical significance.

Fluctuations in the amount of blood loss was estimated by measuring aspirated blood volume and adding the subtracted

FIG. 4. The relationship among the mesoureter, ureter, and surrounding organs. Latzko’s pararectal space, mesoureter, Okabayashi’s pararectal space, and suspensory system are separated. The cardinal ligament is reflected cephalad near to the entrance of the ureteric canal, becoming the mesoureter.

Separation of the ureter within the tunnel is shown with arrows. A, bladder; B, uterus; C, uterine artery; D, ureter; E, fascia of cardinal ligament; F, fascia of mesoureter; G, areolar tissue of mesoureter; H, mesorectum; I, Okabayashi’s pararectal space; J, Latzko’s pararectal space; K, rectouterine ligament; L, uterine roof.

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FIG. 5. Okabayashi’s pararectal space, the medial view in right pelvic cavity. (a) Okabayashi’s pararectal space has just been opened up following separation of the posterior leaf of the broad ligament from the mesoureter still attaching the ureter. (b) Further developing of Okabayashi’s pararectal space until reaching the mesorectum is shown. The hypogastric nerve (arrow 1) is pursued to the lateral ligament (arrow 2). In addition, the rectouterine ligament is shown, having been severed at complete separation. A, ureter; B, posterior leaf of broad ligament; C, mesoureter; D, Okabayashi’s pararectal space; E, Latzko’s pararectal space; F, bladder; G, uterus; H, rectum; I, mesorectum; J, ligated and severed rectouterine ligament.

RESULTS I. Anatomy The anchoring mechanisms of the pelvic organs to the pelvic wall are composed of two traction systems; dorsoventral and lateral pelvic connective tissue. The authors named the former as suspensory system and the latter as supporting system.

A. Suspensory system. The suspensory system is a true musculofascial complex that connects the bladder, uterus, and rectum dorsoventrally. The pubovesical ligament attached to the periosteum of the symphysis pubis fuses with the vesical fascia on the lateral aspect of the bladder, becoming the superficial layer of the vesicouterine ligament [3]. The superficial layer of the vesicouterine ligament fuses with the lateral aspect of the uterine cervical fascia and becomes the rectouterine/

vaginal ligament which fuses with the rectal fascia and, finally, with the sacrum as the rectosacral ligament (Fig. 1).

B. Supporting system. The supporting system (Fig. 2) has both supply-drainage and fascial functions, in addition to enveloping the suspensory system from outside, and it is this connective tissue matrix that anchors the intrapelvic organs to the lateral pelvic wall. The supporting system can be divided into the stem and its reflection, the stem being a ligamentous complex consisting of the lamina ligamenti umbilicalis lateralis [3] and cardinal and lateral ligaments. The complex consisting of the cardinal and lateral ligaments corresponds with Pernkopf’s neurovascular stalk [9, 10]. If one applies present terminology to the reflection, the cephalad reflected plane of the cardinal ligament is the mesoureter [11] and the caudal reflected one the Okabayashi deep layer of vesicouterine liga-

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FIG. 6. Fourth space exposed between superficial layer of the vesicouterine ligament and ureter, the medial view in right pelvic cavity. The arrow shows the uterine roof including the blood vessels and the broken line the point of dissection for the superficial layer of the vesicouterine ligament, respectively. The fourth space theoretically leads into the mesorectum space. A, ureter; B, superficial layer of vesicouterine ligament; C, uterine cervix; D, uterine body; E, bladder; F, paravesical space; G, pararectal space; H, external iliac vessels; I, fourth space.

II. Surgical Techniques

A. Development of the pararectal space and posterior maneuver. Latzko’s pararectal space was developed between the mesoureter and the lateral pelvic wall. Okabayashi’s pararectal space was developed by holding the posterior leaf of the broad ligament with Allis forceps, severing the connective tissue between the ureter and the posterior leaf of the broad ligament, and opening the space between the rectouterine ligament and mesoureter (Fig. 5a). With this maneuver the ureter could be seen to be attached to the medial aspect of the mesoureter.

Okabayashi’s pararectal space communicates with the space which lies deeply between the rectum and the mesorectum, and the hypogastric nerve can be observed at the bottom (Figs. 4 and 5b).

The sacro/rectouterine ligament which is separated in the space between Okabayashi’s pararectal space and rectouterine septum (space) can be dissected separately from the cardinal ligament (Fig. 5b). Freeing of the ureter from the suspensory system is important for unroofing of the ureter in its tunnel (arrow, Fig. 4).

An operative procedure was designed in which a space was developed surgically between the suspensory and the supporting systems, both of which were separated, and each was dissected independently.

B. Development of the fourth space and anterior maneuver.

The method of developing this space is demonstrated as follows: After retracting the exposed bladder toward the symphysis pubis with the vaginal bladder spatula and applying ceph-

ment [6], respectively. There is no accurate corresponding terminology for the reflected plane of the lateral ligament and lamina ligamenti umbilicalis lateralis, but the latter is often regarded as the deep layer of the vesicouterine ligament of Okabayashi.

C. Relationship between the suspensory/supporting system and spaces. An artificial space can be developed between the supporting and the suspensory systems (Fig. 3); one is the Okabayashi pararectal space and the other a new space which corresponds to the paravesical space, the latter being called the fourth space. The bundle that lies between the fourth and paravesical spaces is a combination of the reflected plane of the lamina ligamenti umbilicalis lateralis and deep layer of the vesicouterine ligament of Okabayashi. This bundle makes a pair with the mesoureter and acts as a direct or indirect pathway for the ureteric rami of the internal iliac vessels (Fig. 4).

Further, the ureter and autonomic nerve run to the bladder between the two systems through this space (Fig. 3).

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FIG. 7. Perforation of the reflection of lamina ligamenti umbilicalis lateralis, the medial view in right pelvic cavity. It is understood that the reflection of lamina ligamenti umbilicalis lateralis and mesoureter have a symmetrical structure surrounding the stem of cardinal ligament. Excessive bleeding accompanying vesicouterine ligament dissection is caused by damage to the deep uterine vein and its drainage branches. A, ureter; B, reflection of the lamina ligamenti umbilicalis lateralis; C, mesoureter; D, deep uterine vein; E, external iliac vessels; F, uterus; G, rectum; H, paravesical space.

alad traction to the uterus, the superficial layer of the vesicouterine ligament is exposed (Figs. 3 and 6).

While holding and stretching the mid-segment of the tense superficial layer of the vesicouterine ligament with Allis forceps, the roof of the fascial tunnel is coagulated and sheared along the lateral margin of the superficial layer of the vesicouterine ligament. With the emerging ureter as a target and by repeated coagulation and shearing of the loose connective tissue the fourth space is developed (Fig. 6). Then the remains of the ureteric roof including the blood vessels at the entrance to the ureteric tunnel are ligated and severed (arrow, Fig. 6).

Development of the fourth space is complete when it is extended to the vesicoureteric junction.

Next, by lifting the ureter, the tense reflection of lamina ligamenti umbilicalis lateralis is perforated by Kelly’s forceps through the fourth space to the paravesical space; it is then ligated and dissected (Fig. 7). During this maneuver excessive bleeding will occur if the deep uterine vein crossing under the ureter is damaged. With this maneuver the ureter is completely separated from the cardinal ligament, and the cardinal ligament and bladder remain connected only by the deep layer of the vesicouterine ligament of Okabayashi.

In order to preserve the vesical nerve branch, dissection of the deep layer of the vesicouterine ligament is carried out by

severing only the superior vesical vein which connects the bladder and deep uterine vein within the deep layer of the vesicouterine ligament [2, 12]. Dissection of the cardinal ligament is, then, completed by severing the separated deep uterine vein at the junction of the internal iliac vein. Finally, the superficial layer of the vesicouterine ligament is dissected between the uterine cervix and bladder (broken line, Fig. 6).

Figure 8 shows the state in which the parametrium is dissected, the hypogastric nerve (arrow 1), the lateral ligament including the pelvic nerve plexus (arrow 2), and the deep layer of the vesicouterine ligament including the vesical nerve branch (arrow 3) can be tracked as a route for the continuous pathway of the pelvic nerves.

III. Results of the Operation The amount of blood loss during dissection of the vesicouterine ligament between January 1996 and July 1999 was as follows: 307.7 ⫾ 228.8 ml during the planning stage (n ⫽ 10), 485.0 ⫾ 190.8 ml during the trial stage (n ⫽ 10), and 260.1 ⫾ 114.8 ml during the implementation stage (n ⫽ 13). The implementation stage showed a significant decrease (P ⫽ 0.028) compared to the planning stage.

Comparison of the postoperative urodynamic study between

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FIG. 8. Pathway of the autonomic nerves within the pelvis, the lateral view in right pelvic cavity. Dissection of the parametrial connective tissue leaves only the rectovaginal ligament. The lateral ligament connecting to the rectum is preserved. The hypogastric nerve (arrow 1), lateral ligament including the pelvic nerve plexus (arrow 2), and deep layer of the vesicouterine ligament including the vesical nerve branch (arrow 3) are shown. A, hypogastric nerve; B, lateral ligament of rectum; C, Okabayashi’s deep layer of the vesicouterine ligament; D, fourth space; E, paravesical space; F, pararectal space; G, rectovaginal space; H, stumps of rectouterine ligament; I, uterus; J, bladder; K, external iliac artery.

the planning and the implementation stages is shown in Table 2. There were no cases of low compliance (⬍10) of the bladder. However, all cases in the planning stage and 50% of the implementation stage showed no to low slope in vesical pressure profile in the storage phase. In the voiding phase, voiding with abdominal pressure was observed in 50% of the planning phase and 46.7% of the implementation stage. However, all 23 patients showed good uroflow and an allowable TABLE 2 Five or More Year Survival Rate (Survivals/Operated Cases) (1985–1995)

Stage pT1a a pT1b1 pT1b2 pT2a pT2b pT3a,3b b a b

Survival rate (%) 100 (9/9) 100 (12/12) 85.7 (6/7) 75.0 (6/8) 83.3 (10/12) 75.0 (6/8)

94.7

80.0 75.0

Rate of positive nodes per patient

Mortality of patients with positive nodes

0 0 14.3 (1/7) 25.0 (2/8) 33.3 (4/12) 62.5 (5/8)

0 0 100 (1/1) 0 25.0 (1/4) 40.0 (2/5)

Micro-invase of cervical adenocarcinoma.

Accompanied neoadjuvant chemotherapy.

amount of residual urine. In addition, two patients of the implementation stage showed dysuria only early in the morning for more than 3 months and indicated a low compliance of 10.8 and 14.0. Sphincter activity during urination was observed on a sphincter electromyogram and they were diagnosed with a slight detrusor sphincter dyssynergia. These two patients underwent a drastic clearance around the autonomic nerve by use of an ultrasonic surgical aspirator. An example is shown as Fig. 8.

The number of days required for the amount of residual urine to become less than 50 ml for 33 patients was 13.5 (10.7).

No patient complained of urinary incontinence.

DISCUSSION It is our belief from long surgical experience that the uterus can theoretically be excised if spaces are developed between the parametria and emerging bundles are dissected in sequence.

Our aim was to carry out such a procedure by preserving adjacent organs, while incorporating a high rate of safety, precision, and radicality. The amount of blood loss during the anterior maneuver could be reduced by avoiding damage to the venous system by an understanding of the relationship between

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FIG. 9. Uterine artery/vein and ureter. The deep layer of the vesicouterine ligament is shown from the inner aspect of the cardinal ligament. The ureter is sandwiched between the uterine artery and the deep uterine vein. Separation of the ureter is the salient aspect of cardinal ligament dissection. The pathway for the vesical nerve branch is shown along the branch of the deep uterine vein within the deep layer of the vesicouterine ligament. A, uterine artery; B, deep uterine vein; C, middle rectal artery/vein; D, superior vesical vein; E, pelvic nerve plexus; F, ureter; G, caudal reflection of supporting system; H, uterine cervix.

the branch of the deep uterine vein within the reflection of the neurovascular stalk and the ureter (Fig. 9). As a result of this anatomic knowledge, the mean (SD) total amount of blood loss in radical hysterectomy was 850.0 ⫾ 290.0 ml from 1987 to 1988 [1], 592.0 ⫾ 238.2 ml from 1993 to 1995 [2], and 561.0 ⫾ 243.5 ml from January 1998 to March 1999. These results imply that our concept regarding anatomy and application of it to our operative techniques is promising.

Seeing Okabayashi’s pararectal space from a new aspect and discovery of the fourth space have embodied further the pathway for the autonomic nerves and made the results predictable.

However, in a few cases, delay in complete postoperative recovery of bladder function was evident. If we define maximum cystometric capacity and compliance as parameters for the storage function and residual urine, maximum flow rate and maximum detrusor pressure as parameters for the voiding function, then, out of 23 patients, the number of patients with normal storage function was 20 (87.0%) and that with normal voiding function was 13 (56.5%). These data suggest a higher dysfunction on the part of the parasympathetic nerve. Our

operative procedure is theoretically considered to give less localized damage to the pelvic splanchnic nerves and pelvic nerve plexus because of preservation of the lateral ligament (Fig. 8). The difference in dysfunction between the sympathetic and parasympathetic nerves at the periphery of the pelvic nerve plexus may be due to a difference in the pathway of the nerve within the deep layer of the vesicouterine ligament and/or a difference in sensitivity to surgical stimuli, though, in our experience. Therefore, in order to preserve the bladder function, minimal damage to the ureterovesical branch is required (Fig. 9). Total preservation of the mesoureter and reflection of the lamina ligamenti umbilicalis laterals is one such measure that can possibly and technically be accomplished as shown in Fig. 7. However, preservation of this tissue and radicality have an antinomic relationship, requiring a detailed follow-up regarding prognosis. Further, in order to prevent any nerve damage, preparation of the tissues along the autonomic nerve pathway and reflection of the lamina ligamenti umbilicalis lateralis needs to be carried out using surgical suction instead of the ultrasonic surgical aspirator [13].

Yagi [14], who directly inherited the Okabayashi procedure, improved survival rates for stage I (90.9% for stage I and 61.7% for stage II). Magara et al. [15], who performed a thorough clearance of the origin of the cardinal ligament, was successful in improving survival rates for stage II (94.1% for stage I and 83.3% for stage II). We were successful in achieving high safety and radicality with preserving the pelvic nerve plexus by leaving the lateral ligament intact (Table 2). Further, in this study we restructured the method for parametrial dissection with a two-connective tissue system according to its characteristics and function instead of the traditional threeligament system, with the intention of sending a message to the next generation of gynecologists.

When designing a surgical method for laparoscopic abdominal radical hysterectomy the greatest difficulty will not be encountered in the dissection of the cardinal ligament but in the unroofing of the ureter and dissection of the deep layer of vesicouterine ligament. Because of this we need to avoid ligature en masse of the ligament, and to isolate each individual blood vessel. We believe that the development of our theory of new spaces according to reclassification of the parametrium and a detailed pathway for the deep uterine vein will serve as an aid in the further development of laparoscopic surgery.

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REEXAMINATION OF THE PARAMETRIUM AND SPACE 4. Peham HV, Amreich J: Gyna¨kologische Operationslehre. Karger, Berlin, 1930, pp 350 –385 5. Okabayashi H: Radical abdominal hysterectomy for cancer of the cervix uteri. Surg Gynecol Obstet 33:335–341, 1921 6. Okabayashi H: Abdominale systematische Panhysterektomie fu¨r Karzinom des Uterus. Jpn J Obstet Gynecol 11:136 –153, 1928 [German] 7. Uhlenhuth E, Day EC, Smith RD, Middleton EB: The visceral endopelvic fascia and the hypogastric sheath. Surg Gynecol Obstet 86:9 –28, 1948 8. Machida T: Urological therapy, in Questions and Answers, 18th ed. Roppo Publications, Tokyo, 1998, pp 1064 –1115 9. Pernkopf E: Topographische Anatomie des Menschen. Zweiter Band, Urban und Schwarzenberg, Berlin, 1943, pp 191–197 10. Platzer W: Pernkopf Anatomy: Topographic and Applied Human Anat-

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omy, 3rd ed. Urban und Schwarzenberg, Baltimore-Munich, 1989, pp 284 –302 11. Ka¨ser O, Ikle FA: Gynecologic Operations. Grune & Stratton, New York, 1967, pp 242–261 12. Yabuki Y: Cardinal ligament dissection based on a new theory, C.M.E. J Gynecol Oncol 2:278 –287, 1997 13. Ho¨ckel M, Konerding MA, Heussel CP: Liposuction assisted nervesparing extended radical hysterectomy: Oncologic rationale, surgical anatomy, and feasibility study. Am J Obstet Gynecol 178:971–976, 1998 14. Yagi H: Treatment of carcinoma of the cervix uteri. Surg Gynecol Obstet 95:552–556, 1952 15. Magara M, Iwaya H, Senda T: Abdominal radical operation for cancer of the cervix. Oncology 21:283–299, 1967