Dissection of the cardinal ligament in radical hysterectomy for cervical cancer with emphasis on the lateral ligament Yoshihiko Yabuki, MD, Akihiro Asamoto, MD, Tsutomu Hoshiba, MD, Hideaki Nishimoto, MD, and Shuichi Kitamura, MD Kanazawa, Japan Surgical experience with carcinomas of the uterus and rectum has provided new insights into the surgical anatomy of a lamina, which separates the paravesical space from the pararectal space. It has been proved that each of the lamina consists of the cardinal and lateral ligaments and pelvic splanchnic nerves, descending in the following order. The cardinal and lateral ligaments, as a connective stalk, insert into the lateral walls of the uterus and rectum extending from the inner aspect of the pelvic wall. Clarification of this structural relationship led to the development of a new procedure for the dissection of the cardinal ligament in radical hysterectomy, while still preserving the lateral ligament. This facilitated systematic dissection of the cardinal and uterosacral ligaments with posterior manipulation, leading to a reduction in blood loss and to prevention of brisk bleeding from the venous plexuses. (AM J OBSTET GVNECOL 1991 ;164:7-14.)
Key words: Cardinal ligament; lateral ligament; radical hysterectomy; cervical cancer; ultrasonic surgical aspirator
Dissection of the cardinal ligament is one of the most critical procedures in radical hysterectomy, requiring skills of the highest degree. Over the years this procedure has been greatly influenced by individual surgeons and the differences in their techniques. The 5year survival rate of patients who have surgical treatment for uterine cancer has already peaked' and to improve it there must be a narrowing of these differences and safer techniques. Today's dissection of the cardinal ligament owes much to the groundwork of Latzko (1919); Okabayashi (1921),3 and Meigs (1944)' who improved the original Wertheim operation. 5 They had a common factor in their surgical procedure, which was to expose the paravesical and pararectal spaces and then separate the retinaculum uteri into pars anterior, medial, and posterior, followed by resection of each pars individually. This made systematic and extensive resection of the parametrial ligament possible. With regard to the cardinal ligament dissection, Meigs 6 improved the Wertheim operation in a comparatively orthodox manner by mere dissection of the Mackenrodt ligament, whereas Latzk0 7 and Okabayashi3 . 8 pursued a radical approach by resection of the ligament, lateral stalk of the pelvis, deep down in the pelvic floor. This procedural difference made definiFrom the Department of Obstetrics and Gynaecology, Ishikawa Prefectural Central Hospital. Reprint requests: Yoshihiko Yabuki, MD, Department of Obstetrics and Gynaecology, Ishikawa Prefectural Central Hospital, MinamiShinbo Nu 153, Kanazawa, Japan 920-02.
6/1 /22987
tion of the cardinal ligament unclear. Specifically, the anatomy and operative manipulation of the inferior border of the cardinal ligament was not always clearly defined. An operation performed with the boundaries of the base of the ligament and its adjacent organs undefined is in danger of damaging blood vessels and nerves by invasion into adjacent tissues. Especially, unskilled technique may cause an unexpected massive hemorrhage. Kobayashi9 . 10 improved the Latzko and Okabayashi operation by separating the cardinal ligament into the pars nervosa and pars vasculosa after opening the paravesical and pararectal spaces completely to the superior surface of the levator ani so that the vesicular function was preserved by leaving the pars nervosa behind. This manipulation made more detailed explanation of the anatomy of the cardinal ligament very clear, but it was not stated why a part of it remained in the pelvirectal space. With a view to further understanding the relationship between the parametrium and paraproctium, we performed operations for advanced rectal cancer and came to the following conclusions"' 12: (1) Metastasis of the cardinal lymph nodes found in many advanced rectal cancers suggested some continuity between the parametrium and paraproctium, and (2) After an anterior resection of the rectum together with a radical hysterectomy, a view of the dissected end of the ligament on the inner aspect of the pelvic wall is the same as that by radical hysterectomy with a simultaneous resection of the pars vasculosa and pars nervosa (i.e., the Oka7
8 Yabuki et al.
January 1991 Am J Obstet Gyneco1
CoI1'
Cervix
c
Fig. 1. Left, specimen removed by combination of rectal transection and radical hysterectomy for rectal cancer. Right, Severed ends on lateral wall of pelvis. Cardinal and lateral ligaments form laminae supporting uterus and rectum. A, Deep uterine vein and its severed end; B, lateral ligament and severed end of middle rectal artery and vein; C, connective tissue containing pelvic splanchnic nerves.
bayashi operation). This finding coincides with that of a deep pelvic dissection with total pelvic exenteration reported by Mattingly.13 Furthermore, when dissecting the cardinal ligament, the visceral branch of the internal iliac vessels (i.e., the deep uterine vein and middle rectal vessels) are exposed at their bifurcation and followed up to the runnings. The results led us to make the following inferences12: (I) In conventional radical hysterectomy,3, 7, 9, 14, 15 the Mackenrodt ligament and lateral ligament, '6 which connects the rectum to the posterolateral pelvic wall, in which the middle rectal· vessels pass at the level of the third sacral vertebra, have not been clearly differentiated, and (2) So-called cardinal ligament excised in many conventional radical hysterectomies may be a combined connective stalk consisting of the Mackenrodt and lateral ligaments and sometimes even the pelvic splanchnic nerves. These inferences are necessary to clarify the anatomic relationship among the cardinal and lateral ligaments and pelvic splanchnic nerves. To our knowledge, no, textbook of gynecosurgical procedures or
anatomy is available that describes these two ligaments in a mutually related manner. Only the concept of Gefa~-Nerven-Leitplattedes Beckens as described by E. PernkopP7 (connective stalk, coated with visceral pelvic fascia, connects the lateral pelvic wall and the organs of the lesser pelvis) gives any suggestions similar to our opinions about the cardinal ligament. In this article we describe our method of dissecting the cardinal ligament on the basis of the knowledge and findings of the surgical anatomy of the cardinal and lateral ligaments derived from operations for rectal cancer. It is hoped that our hypotheses will stimulate discussions among the readership on this matter and further verifications will be pursued.
Method Subjects consisted of 41 patients with uterine cancer and 10 patients with rectal cancer on which we performed radical hysterectomy. In accordance with the Okabayashi-Meigs method, radical hysterectomy for uterine or rectal cancer was carried out by the following procedure: abdominal incision, severance of the round
Volume 164 Number 1, Part 1
and pelvic infundibular ligaments, open the peritonium to the iliac fossa, exposure of the paravesical and pararectal spaces, dissection of the intrapelvic lymph nodes, manipulation of the opposite side, separation and severance of the uterine artery, isolation of the ureter, separation and severance of the cardinal ligament, manipulation of the opposite side, separation of the rectum from the uterus, severance of the uterosacral and reetovaginal ligaments, manipulation of the opposite side, separation of the bladder, separation and severance of the superficial and deep layers of the vesicouterine ligament, resection of the paravaginal connective tissue, manipulation of the opposite side, transection of the vagina, and closure. Separation and removal of the cadinalligament and lymphatic tissues were carried out in part with an ultrasonic surgical aspirator (Cavitron Surgical Systems Inc., Stamford, Conn.). The operative condition of the ultrasonic surgical aspirator was as follows: an ultrasound frequency of 150 to 210 fLm with a suction pressure of 200 to 400 mm Hg and an irrigation rate of 30 to 40 cc per minute. The Student t test was used to determine whether there was a significant difference in blood loss between patients who underwent radical hysterectomy before 1985 and those after 1987. The level of significance was set at 0.05 a.-level. With consideration of the Japanese physique, we used the modified Broca index of weight/(height - 100) X 0.9 to express the degree of obesity.
Reappraisal of cardinal ligament dissection
9
,
c
Results
Surgicoanatomic relationship between the cardinal and lateral ligaments. Fig. 1 shows the specimen tissue for rectal cancer and its pelvic severed end. The operation was carried out by rectal transection and radical hysterectomy. Intraoperative observation and postoperative angiography of the surgical specimen showed that the vessels on the photomicrograph of the dissected ligament (Fig. 2) are in the following descending order: uterine artery, deep uterine vein, and middle rectal artery and vein. These findings indicate that the cardinal and lateral ligaments and pelvic splanchnic nerves form a lamina, as schematically shown in Fig. 3, which connects the uterus and rectum with the lateral inner aspect of the pelvic wall. The space caudal to the lamina is the paravesical space (actually the paravesical fossa and caudal part of the pararectal fossa), whereas the one that is on the cranial side is the pararectal space (actually the cranial part of the pararectal fossa). All major blood vessels in the lamina are visceral branches of the internal iliac vessel in which the uterine artery and the superficial and deep uterine veins pass through the cardinal ligament, whereas the middle rectal artery and vein pass through the lateral ligament. As shown in Fig. 4, the deep uterine vein passes through the cardinal ligament at the level of the ischial
Fig. 2. Photomicrograph of resected laminae. (Elastica van Gieson stain: x 1.) A, Uterine artery; B, deep uterine vein; C, middle rectal artery; D, middle rectal vein; and E, pelvic splanchnic nerves.
spine and joins the internal iliac vein. The middle rectal artery branches mainly from the common trunk of the inferior gluteal and internal pudendal arteries and travels inferiorly along the deep uterine vein to the side of the rectum. The middle rectal vein passes through a similar course with a number of aberrations. Dissection of the cardinal ligament. When the operation has proceeded as far as isolation of the ureter, the lamina becomes visible resembling a bridge spanning the paravesical and pararectal spaces. The dissection of the cardinal ligament commences with a resection of the strong fibrous tissue, that is, fascia pelvis visceralis as described by E. Pernkopf, 17 constituting the anterior and posterior surfaces of the lamina. This fibrous tissue is separated and severed accordingly. After removal of the fascia, the intraligamentallymph nodes and fibrous and fatty areolar tissues are removed with a pair of hookless dissecting forceps and an ultrasonic surgical aspirator or a surgical suction apparatus at a pressure of approximately 200 mm Hg, thereby re-
10
Yabuki at al.
January 1991 Am J Obstet Gynecol
Fig. 3. Laminae connecting pelvic inside of wall with uterus and rectum (view from sacral side). A, Paravesical space; B, pararectal space; C, uterus; D, rectum; E, cardinal ligament containing uterine artery and vein; F, lateral ligament containing middle rectal artery and vein; and G, pelvic splanchnic nerves.
'I
Fig. 4. Illustration indicates relationship between visceral branches of internal iliac vessel with uterus and rectum. Deep uterine vein does not join directly into uterine cervix, but forms stalk with middle rectal artery and vein. 1, Internal iliac artery and vein; 2, umbilical artery; 3, uterine artery; 4, deep uterine vein; 5, middle rectal artery and vein; 6, pelvic splanchnic nerves; 7, uterus, and 8, rectum.
vealing the deep uterine vein and the lateral ligament containing the middle rectal vessel and neural part below it (Fig. 5). The exposed deep uterine vein and lateral ligament
are separated from each other by insertion of Kelly's forceps. The former is ligated and severed on the pelvic side of the vessel's bifurcation (Fig. 6). The uterine side of the severed end of the deep uterine vein is raised,
Reappraisal of cardinal ligament dissection
Volume 164 Number I, Part 1
Int.
111 C rt.
P rar Ct rio
v 1n
8p (Cr
Cl
11
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1 1 part)
Slump of faac1a peivia
viaceral1a
Par v a1c 1 ap c
Fig. 5. Excision of fascia covering ligaments after developing paravesical space and pararectal space exposes vascular part and part of connective tissue. According to standard method for cardinal ligament dissection as used in Japan, ligaments are cut through a tunnel constructed between pars vasculosa and pars nervosa or beneath pars nervosa.
separating its distal segment from the lateral ligament up to the uterine cervix. In this way, both the cardinal and lateral ligaments are separated in their entirety and the rectovaginal ligament appears at the separated end (arrow, Fig. 4). At this time, care must be taken of hemorrhaging as a result of invasion into the rectouterine venous plexus. Finally, tissues surrounding the lateral ligament are adequately removed by the use of a ultrasonic surgical aspirator, completing the dissection of the cardinal ligament. The tissue specimen (Fig. 7) removed by the conventional method is compared with that removed by the lateral ligament saving method. In the latter case the pelvic splanchnic nerves remain intact. Benefits of the new surgical procedure. The amount of blood loss was measured at 30-minute intervals in 20 patients who underwent standard radical hysterectomy before 1985, at which time we realized the presence of the lateral ligament. Two years after the estab-
lishment of our new operative measure from 1987 through 1988 we did a comparison of blood loss on 21 patients with that of the prior group of 20 patients (Fig. 8). Table I shows operative information on patients of both groups. The time course of the operative procedure was judged from the anesthetic record, the intraoperative photographing time, and our operative speed experience. Blood loss during cardinal ligament dissection was significantly reduced in the latter group for the following reasons: (I) clarification of laminae anatomy by means of ultrasonic surgical aspirators; (2) avoidance of complete exposure of the pararectal space by disclosure of the superior surface of the levator ani only as required in the standard radical hysterectomy; and (3) systematization of posterior manipulations such as dissection of the uterosacral ligament (Fig. 9) because of the preservation of the lateral ligament. These improvements led to the prevention of intraligamental rupture of vessels and breakage of the venous plexuses
12
Yabuki at al.
January 1991 Am J Obstet Gynecol
Ext.
11iac:. art. , vein
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Fig. 6. Middle rectal artery and vein that become visible after severance of deep uterine vein.
-----
--
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Fig. 7. Left, Specimen removed by conventional dissection of the cardinal ligament for cervical cancer. Right, Specimen removed by our lateralligament-pteserving method. Conventional technique leaves cut-end mass of ligament in pelvic wall, posing problems for curability.
r )
Reappraisal of cardinal ligament dissection
Volume 164 Number 1, Part 1
A
Ul
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._ >
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B
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120 150 180 210 240 270 300 330 Time (minutes)
Fig. 8. Comparison of intraoperative bleeding measured at 30-minute intervals, between standard radical hysterectomy (total volume, 1092 ± 359 ml; operation time, 300 ± 32 minutes) and radical hysterectomy with our method (total volume, 850 ± 290 ml; operation time 296 ± 36 minutes). In the latter case blood losses measured at 120 and ISO minutes were 75 ± 27 and 86 ± 44 ml, respectively. These values are significantly smaller than counterparts of 127 ± 51 and 158 ± 83 ml for the former (p < 0.05). A, Dissection of intrapelvic lymph nodes; B, dissection of cardinal ligament; C, severance of uterosacral and rectovaginalligaments; D, severance of vesicouterine ligament and paracolpium.
Ut
rus
pl
chnlc
Fig. 9. When cardinal and lateral ligaments are clamped and severed together (arrow A), complete separation between uterus and rectum necessitates severance of not only uterosacral ligament or rectovaginalligament (arrow C) but also attachment of lateral ligament to rectum (arrow B). in the vicinity of the pelvic wall, rectum, and anterior surface of the sacrum.
Comment The difference in the operative procedure of the cardinal ligament dissection among the Wertheim, Meigs, Latzko, and Okabayashi operations is that the former two adopt dissection of the Mackenrodt ligament, whereas the latter adopt deep dissection of the lateral pelvic stalk. The principle of surgical treatment
for cancer necessitates extensive removal of affected tissue while maintaining functions of adjacent organs as much as possible. Although the preservation of the lateral ligament seems inconsistent with a radical cure, no progress will be possible without overcoming this dilemma. Table II shows comparative 5-year survival rates for uterine cancer among the Wertheim and Okabayashi operations as cited from Kobayashi's work,9 and the Meigs operation. 18 A comparison of the values for these
14 Yabuki et al.
January 1991 Am J Obstet Grnecol
Table I. Information on patients who had surgery
Standard method Our new method
Clinical stage
No. of patients
Age (yr)
I
20 21
53.4 :t 8.2 52.6 :t 9.5
4
6
Table II. Comparison of 5-year survival of patients operated on for cervical cancer between the Wertheim, Okabayashi, and Meigs operation --w-er-t-hej-'m--
-----I Stage I Stage II
(%) 64.0 46.6
Broca index
Intraoperative blood transfusion
Blood loss
II
14 17
1.16 :t 0.16 1.07 :t 0.19
955.8 :t 417.4 777.8 :t 642.5
1029 :t 359 850 :t 290
(ml)
REFERENCES
Okabayashi
Meigs
43.3
60.7
(%)
I
(%) ---------90.9 80.7
three operative methods does not always confirm the need for deep pelvic dissection advocated by Okabayashi. In terms of 5-year survival rates for the Wertheim and Okabayashi operations, there was a significant difference for stage I cancers by the Okabayashi operation, but no significant difference for stage II cancers. This was probably because of the dependence of the prognosis on the presence of metastasis in the pelvic lymph nodes irrespective of the operative methods. Our experience further indicated that the Laztko and Okabayashi operations leave the massive severed end of the ligament in the inner aspect of the pelvic wall, posing a problem for recurrence and consequently limiting both operative procedures. Whereas our operation followed the traditional procedure of the Okabayashi operation, it is characterized by its concise anatomy of the depth of the laminae (socalled cardinal ligament) and by a complete extirpation of the cardinal ligament (the Mackenrodt ligament) from the pelvic wall after exposure and resection of the cardinal blood vessels at the bifurcation of the trunk. In this case, an ultrasonic surgical aspirator is highly contributive. However, when an ultrasonic surgical aspirator is used, complete irrigation and suction throughout the operative field are imperative to eliminate the risk of disseminating viable malignant cells. '9 Furthermore, careful attention should be paid to prevent nerve injury as a result of the ultrasound and heated tip of the ultrasonic surgical aspirator. In conclusion, our anatomic opinions on the cardinal ligament will also be of interest to surgeons who carry out operations for advanced rectal cancer or gynecologists who perform uterine transplantation in addition to operations for uterine cancer.
1. Twenty-eighth annual report on the results of treatment in carcinoma of the uterus. Noda K, ed. Acta Obstet GynaecolJpn 1988;44:271-310. 2. Latzko W, Schiffmann J. Zur Klinik und Anatomie der erweiterten abdominallen Operation des Gebarmutterkrebses. Zentralbl Gynaekol 1919;34:715-9. 3. Okabayashi H. Radical abdominal hysterectomy for cancer of the cervix uteri. Surg Gynecol Obstet 1921;33:33541. 4. Meigs JV. Carcinoma of the cervix-the Wertheim operation. Surg Gynecol Obstet 1944;78:195-8. 5. Wertheim E. The extended abdominal operation for carcinoma uteri (based on 500 operative cases). Am J Obstet Dis Women Child 1912;66: 169-232. 6. Meigs JV. Radical hysterectomy for cancer of the cervix with bilateral pelvic lymphadenectomy (the socalled Wertheim operation). In: Progress in gynecology. New York: Grune & Stratton, 1950 vol 2:540-60. 7. Peham HV, AmreichJ. Gynakologische Operationslehre. Berlin: S. Karger, 1930. 8. Okabayashi H. Abdominale systematische Panhysterektomie fur Karzinom des Uterus. Jpn J Obstet Gynecol 1928;11:136-53. 9. Kobayashi T. Abdominal radical hysterectomy with pelvic lymphadnectomy for cancer of the cervix. Tokyo: Nanzando, 1961. 10. Kobayashi T. Preservation of the pelvic parasympathetic nerves in radical hysterectomy for cancer of the cervix. In: Congress edition of the 5th World Congress of Gynecology and Obstetrics. Sandorama, September 1967: 32. 11. Yabuki Y, Asamoto A, Hoshiba T, et aI. Indication of radical hysterectomy for advanced rectal cancer. Operation 1987;42:1475-8. 12. Yabuki Y, Asamoto A, Nishimoto H, et aI. Reappraisal of cardinal ligament dissection in the Okabayashi operation for cervical cancer. In: Congress edition of the 42nd Annual Scientific Meeting of the Japan Society of Obstetrics and Gynecology. Tokyo, April 1990:345. 13. Mattingly RF. Indications, contraindications, and method of total pelvic exenteration. Oncology 1967;21 :241-59. 14. Vagi H. Extended abdominal hysterectomy with pelvic lymphadenectomy for carcinoma of the cervix. AM J 08STET GVNECOL 1955;69:33-47. 15. Nakano R. Abdominal radical hysterectomy and bilateral pelvic lymph node dissections for cancer of the cervix. Gynecol Obstet Invest 1981; 12:281-93. 16. Williams PL, Warwick R, eds. Gray's anatomy. 36th ed. Edinburgh: Churchill Livingstone, 1980. 17. Pernkopf E. Topographische Anatomie des Menschen. Zweiter Band, Berlin: Urban und Schwarzenberg, 1943. 18. Meigs JV. Radical hysterectomy with bilateral pelvic lymph node dissections. AM J 08STET GVNECOL 1951 ;62:854-70. 19. Oosterhuis JW, Lung PF, Verschueren RCJ, Oldhoff J. Viability of tumor cells in the irrigation fluid of the Cavitron Ultrasonic Surgical Aspirator (CUSA) after tumor fragmentation. Cancer 1985;56:368-70.
Key words: Cardinal ligament; lateral ligament; radical hysterectomy; cervical cancer; ultrasonic surgical aspirator
Dissection of the cardinal ligament is one of the most critical procedures in radical hysterectomy, requiring skills of the highest degree. Over the years this procedure has been greatly influenced by individual surgeons and the differences in their techniques. The 5year survival rate of patients who have surgical treatment for uterine cancer has already peaked' and to improve it there must be a narrowing of these differences and safer techniques. Today's dissection of the cardinal ligament owes much to the groundwork of Latzko (1919); Okabayashi (1921),3 and Meigs (1944)' who improved the original Wertheim operation. 5 They had a common factor in their surgical procedure, which was to expose the paravesical and pararectal spaces and then separate the retinaculum uteri into pars anterior, medial, and posterior, followed by resection of each pars individually. This made systematic and extensive resection of the parametrial ligament possible. With regard to the cardinal ligament dissection, Meigs 6 improved the Wertheim operation in a comparatively orthodox manner by mere dissection of the Mackenrodt ligament, whereas Latzk0 7 and Okabayashi3 . 8 pursued a radical approach by resection of the ligament, lateral stalk of the pelvis, deep down in the pelvic floor. This procedural difference made definiFrom the Department of Obstetrics and Gynaecology, Ishikawa Prefectural Central Hospital. Reprint requests: Yoshihiko Yabuki, MD, Department of Obstetrics and Gynaecology, Ishikawa Prefectural Central Hospital, MinamiShinbo Nu 153, Kanazawa, Japan 920-02.
6/1 /22987
tion of the cardinal ligament unclear. Specifically, the anatomy and operative manipulation of the inferior border of the cardinal ligament was not always clearly defined. An operation performed with the boundaries of the base of the ligament and its adjacent organs undefined is in danger of damaging blood vessels and nerves by invasion into adjacent tissues. Especially, unskilled technique may cause an unexpected massive hemorrhage. Kobayashi9 . 10 improved the Latzko and Okabayashi operation by separating the cardinal ligament into the pars nervosa and pars vasculosa after opening the paravesical and pararectal spaces completely to the superior surface of the levator ani so that the vesicular function was preserved by leaving the pars nervosa behind. This manipulation made more detailed explanation of the anatomy of the cardinal ligament very clear, but it was not stated why a part of it remained in the pelvirectal space. With a view to further understanding the relationship between the parametrium and paraproctium, we performed operations for advanced rectal cancer and came to the following conclusions"' 12: (1) Metastasis of the cardinal lymph nodes found in many advanced rectal cancers suggested some continuity between the parametrium and paraproctium, and (2) After an anterior resection of the rectum together with a radical hysterectomy, a view of the dissected end of the ligament on the inner aspect of the pelvic wall is the same as that by radical hysterectomy with a simultaneous resection of the pars vasculosa and pars nervosa (i.e., the Oka7
8 Yabuki et al.
January 1991 Am J Obstet Gyneco1
CoI1'
Cervix
c
Fig. 1. Left, specimen removed by combination of rectal transection and radical hysterectomy for rectal cancer. Right, Severed ends on lateral wall of pelvis. Cardinal and lateral ligaments form laminae supporting uterus and rectum. A, Deep uterine vein and its severed end; B, lateral ligament and severed end of middle rectal artery and vein; C, connective tissue containing pelvic splanchnic nerves.
bayashi operation). This finding coincides with that of a deep pelvic dissection with total pelvic exenteration reported by Mattingly.13 Furthermore, when dissecting the cardinal ligament, the visceral branch of the internal iliac vessels (i.e., the deep uterine vein and middle rectal vessels) are exposed at their bifurcation and followed up to the runnings. The results led us to make the following inferences12: (I) In conventional radical hysterectomy,3, 7, 9, 14, 15 the Mackenrodt ligament and lateral ligament, '6 which connects the rectum to the posterolateral pelvic wall, in which the middle rectal· vessels pass at the level of the third sacral vertebra, have not been clearly differentiated, and (2) So-called cardinal ligament excised in many conventional radical hysterectomies may be a combined connective stalk consisting of the Mackenrodt and lateral ligaments and sometimes even the pelvic splanchnic nerves. These inferences are necessary to clarify the anatomic relationship among the cardinal and lateral ligaments and pelvic splanchnic nerves. To our knowledge, no, textbook of gynecosurgical procedures or
anatomy is available that describes these two ligaments in a mutually related manner. Only the concept of Gefa~-Nerven-Leitplattedes Beckens as described by E. PernkopP7 (connective stalk, coated with visceral pelvic fascia, connects the lateral pelvic wall and the organs of the lesser pelvis) gives any suggestions similar to our opinions about the cardinal ligament. In this article we describe our method of dissecting the cardinal ligament on the basis of the knowledge and findings of the surgical anatomy of the cardinal and lateral ligaments derived from operations for rectal cancer. It is hoped that our hypotheses will stimulate discussions among the readership on this matter and further verifications will be pursued.
Method Subjects consisted of 41 patients with uterine cancer and 10 patients with rectal cancer on which we performed radical hysterectomy. In accordance with the Okabayashi-Meigs method, radical hysterectomy for uterine or rectal cancer was carried out by the following procedure: abdominal incision, severance of the round
Volume 164 Number 1, Part 1
and pelvic infundibular ligaments, open the peritonium to the iliac fossa, exposure of the paravesical and pararectal spaces, dissection of the intrapelvic lymph nodes, manipulation of the opposite side, separation and severance of the uterine artery, isolation of the ureter, separation and severance of the cardinal ligament, manipulation of the opposite side, separation of the rectum from the uterus, severance of the uterosacral and reetovaginal ligaments, manipulation of the opposite side, separation of the bladder, separation and severance of the superficial and deep layers of the vesicouterine ligament, resection of the paravaginal connective tissue, manipulation of the opposite side, transection of the vagina, and closure. Separation and removal of the cadinalligament and lymphatic tissues were carried out in part with an ultrasonic surgical aspirator (Cavitron Surgical Systems Inc., Stamford, Conn.). The operative condition of the ultrasonic surgical aspirator was as follows: an ultrasound frequency of 150 to 210 fLm with a suction pressure of 200 to 400 mm Hg and an irrigation rate of 30 to 40 cc per minute. The Student t test was used to determine whether there was a significant difference in blood loss between patients who underwent radical hysterectomy before 1985 and those after 1987. The level of significance was set at 0.05 a.-level. With consideration of the Japanese physique, we used the modified Broca index of weight/(height - 100) X 0.9 to express the degree of obesity.
Reappraisal of cardinal ligament dissection
9
,
c
Results
Surgicoanatomic relationship between the cardinal and lateral ligaments. Fig. 1 shows the specimen tissue for rectal cancer and its pelvic severed end. The operation was carried out by rectal transection and radical hysterectomy. Intraoperative observation and postoperative angiography of the surgical specimen showed that the vessels on the photomicrograph of the dissected ligament (Fig. 2) are in the following descending order: uterine artery, deep uterine vein, and middle rectal artery and vein. These findings indicate that the cardinal and lateral ligaments and pelvic splanchnic nerves form a lamina, as schematically shown in Fig. 3, which connects the uterus and rectum with the lateral inner aspect of the pelvic wall. The space caudal to the lamina is the paravesical space (actually the paravesical fossa and caudal part of the pararectal fossa), whereas the one that is on the cranial side is the pararectal space (actually the cranial part of the pararectal fossa). All major blood vessels in the lamina are visceral branches of the internal iliac vessel in which the uterine artery and the superficial and deep uterine veins pass through the cardinal ligament, whereas the middle rectal artery and vein pass through the lateral ligament. As shown in Fig. 4, the deep uterine vein passes through the cardinal ligament at the level of the ischial
Fig. 2. Photomicrograph of resected laminae. (Elastica van Gieson stain: x 1.) A, Uterine artery; B, deep uterine vein; C, middle rectal artery; D, middle rectal vein; and E, pelvic splanchnic nerves.
spine and joins the internal iliac vein. The middle rectal artery branches mainly from the common trunk of the inferior gluteal and internal pudendal arteries and travels inferiorly along the deep uterine vein to the side of the rectum. The middle rectal vein passes through a similar course with a number of aberrations. Dissection of the cardinal ligament. When the operation has proceeded as far as isolation of the ureter, the lamina becomes visible resembling a bridge spanning the paravesical and pararectal spaces. The dissection of the cardinal ligament commences with a resection of the strong fibrous tissue, that is, fascia pelvis visceralis as described by E. Pernkopf, 17 constituting the anterior and posterior surfaces of the lamina. This fibrous tissue is separated and severed accordingly. After removal of the fascia, the intraligamentallymph nodes and fibrous and fatty areolar tissues are removed with a pair of hookless dissecting forceps and an ultrasonic surgical aspirator or a surgical suction apparatus at a pressure of approximately 200 mm Hg, thereby re-
10
Yabuki at al.
January 1991 Am J Obstet Gynecol
Fig. 3. Laminae connecting pelvic inside of wall with uterus and rectum (view from sacral side). A, Paravesical space; B, pararectal space; C, uterus; D, rectum; E, cardinal ligament containing uterine artery and vein; F, lateral ligament containing middle rectal artery and vein; and G, pelvic splanchnic nerves.
'I
Fig. 4. Illustration indicates relationship between visceral branches of internal iliac vessel with uterus and rectum. Deep uterine vein does not join directly into uterine cervix, but forms stalk with middle rectal artery and vein. 1, Internal iliac artery and vein; 2, umbilical artery; 3, uterine artery; 4, deep uterine vein; 5, middle rectal artery and vein; 6, pelvic splanchnic nerves; 7, uterus, and 8, rectum.
vealing the deep uterine vein and the lateral ligament containing the middle rectal vessel and neural part below it (Fig. 5). The exposed deep uterine vein and lateral ligament
are separated from each other by insertion of Kelly's forceps. The former is ligated and severed on the pelvic side of the vessel's bifurcation (Fig. 6). The uterine side of the severed end of the deep uterine vein is raised,
Reappraisal of cardinal ligament dissection
Volume 164 Number I, Part 1
Int.
111 C rt.
P rar Ct rio
v 1n
8p (Cr
Cl
11
1
1 1 part)
Slump of faac1a peivia
viaceral1a
Par v a1c 1 ap c
Fig. 5. Excision of fascia covering ligaments after developing paravesical space and pararectal space exposes vascular part and part of connective tissue. According to standard method for cardinal ligament dissection as used in Japan, ligaments are cut through a tunnel constructed between pars vasculosa and pars nervosa or beneath pars nervosa.
separating its distal segment from the lateral ligament up to the uterine cervix. In this way, both the cardinal and lateral ligaments are separated in their entirety and the rectovaginal ligament appears at the separated end (arrow, Fig. 4). At this time, care must be taken of hemorrhaging as a result of invasion into the rectouterine venous plexus. Finally, tissues surrounding the lateral ligament are adequately removed by the use of a ultrasonic surgical aspirator, completing the dissection of the cardinal ligament. The tissue specimen (Fig. 7) removed by the conventional method is compared with that removed by the lateral ligament saving method. In the latter case the pelvic splanchnic nerves remain intact. Benefits of the new surgical procedure. The amount of blood loss was measured at 30-minute intervals in 20 patients who underwent standard radical hysterectomy before 1985, at which time we realized the presence of the lateral ligament. Two years after the estab-
lishment of our new operative measure from 1987 through 1988 we did a comparison of blood loss on 21 patients with that of the prior group of 20 patients (Fig. 8). Table I shows operative information on patients of both groups. The time course of the operative procedure was judged from the anesthetic record, the intraoperative photographing time, and our operative speed experience. Blood loss during cardinal ligament dissection was significantly reduced in the latter group for the following reasons: (I) clarification of laminae anatomy by means of ultrasonic surgical aspirators; (2) avoidance of complete exposure of the pararectal space by disclosure of the superior surface of the levator ani only as required in the standard radical hysterectomy; and (3) systematization of posterior manipulations such as dissection of the uterosacral ligament (Fig. 9) because of the preservation of the lateral ligament. These improvements led to the prevention of intraligamental rupture of vessels and breakage of the venous plexuses
12
Yabuki at al.
January 1991 Am J Obstet Gynecol
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Fig. 6. Middle rectal artery and vein that become visible after severance of deep uterine vein.
-----
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Fig. 7. Left, Specimen removed by conventional dissection of the cardinal ligament for cervical cancer. Right, Specimen removed by our lateralligament-pteserving method. Conventional technique leaves cut-end mass of ligament in pelvic wall, posing problems for curability.
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Reappraisal of cardinal ligament dissection
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Fig. 8. Comparison of intraoperative bleeding measured at 30-minute intervals, between standard radical hysterectomy (total volume, 1092 ± 359 ml; operation time, 300 ± 32 minutes) and radical hysterectomy with our method (total volume, 850 ± 290 ml; operation time 296 ± 36 minutes). In the latter case blood losses measured at 120 and ISO minutes were 75 ± 27 and 86 ± 44 ml, respectively. These values are significantly smaller than counterparts of 127 ± 51 and 158 ± 83 ml for the former (p < 0.05). A, Dissection of intrapelvic lymph nodes; B, dissection of cardinal ligament; C, severance of uterosacral and rectovaginalligaments; D, severance of vesicouterine ligament and paracolpium.
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Fig. 9. When cardinal and lateral ligaments are clamped and severed together (arrow A), complete separation between uterus and rectum necessitates severance of not only uterosacral ligament or rectovaginalligament (arrow C) but also attachment of lateral ligament to rectum (arrow B). in the vicinity of the pelvic wall, rectum, and anterior surface of the sacrum.
Comment The difference in the operative procedure of the cardinal ligament dissection among the Wertheim, Meigs, Latzko, and Okabayashi operations is that the former two adopt dissection of the Mackenrodt ligament, whereas the latter adopt deep dissection of the lateral pelvic stalk. The principle of surgical treatment
for cancer necessitates extensive removal of affected tissue while maintaining functions of adjacent organs as much as possible. Although the preservation of the lateral ligament seems inconsistent with a radical cure, no progress will be possible without overcoming this dilemma. Table II shows comparative 5-year survival rates for uterine cancer among the Wertheim and Okabayashi operations as cited from Kobayashi's work,9 and the Meigs operation. 18 A comparison of the values for these
14 Yabuki et al.
January 1991 Am J Obstet Grnecol
Table I. Information on patients who had surgery
Standard method Our new method
Clinical stage
No. of patients
Age (yr)
I
20 21
53.4 :t 8.2 52.6 :t 9.5
4
6
Table II. Comparison of 5-year survival of patients operated on for cervical cancer between the Wertheim, Okabayashi, and Meigs operation --w-er-t-hej-'m--
-----I Stage I Stage II
(%) 64.0 46.6
Broca index
Intraoperative blood transfusion
Blood loss
II
14 17
1.16 :t 0.16 1.07 :t 0.19
955.8 :t 417.4 777.8 :t 642.5
1029 :t 359 850 :t 290
(ml)
REFERENCES
Okabayashi
Meigs
43.3
60.7
(%)
I
(%) ---------90.9 80.7
three operative methods does not always confirm the need for deep pelvic dissection advocated by Okabayashi. In terms of 5-year survival rates for the Wertheim and Okabayashi operations, there was a significant difference for stage I cancers by the Okabayashi operation, but no significant difference for stage II cancers. This was probably because of the dependence of the prognosis on the presence of metastasis in the pelvic lymph nodes irrespective of the operative methods. Our experience further indicated that the Laztko and Okabayashi operations leave the massive severed end of the ligament in the inner aspect of the pelvic wall, posing a problem for recurrence and consequently limiting both operative procedures. Whereas our operation followed the traditional procedure of the Okabayashi operation, it is characterized by its concise anatomy of the depth of the laminae (socalled cardinal ligament) and by a complete extirpation of the cardinal ligament (the Mackenrodt ligament) from the pelvic wall after exposure and resection of the cardinal blood vessels at the bifurcation of the trunk. In this case, an ultrasonic surgical aspirator is highly contributive. However, when an ultrasonic surgical aspirator is used, complete irrigation and suction throughout the operative field are imperative to eliminate the risk of disseminating viable malignant cells. '9 Furthermore, careful attention should be paid to prevent nerve injury as a result of the ultrasound and heated tip of the ultrasonic surgical aspirator. In conclusion, our anatomic opinions on the cardinal ligament will also be of interest to surgeons who carry out operations for advanced rectal cancer or gynecologists who perform uterine transplantation in addition to operations for uterine cancer.
1. Twenty-eighth annual report on the results of treatment in carcinoma of the uterus. Noda K, ed. Acta Obstet GynaecolJpn 1988;44:271-310. 2. Latzko W, Schiffmann J. Zur Klinik und Anatomie der erweiterten abdominallen Operation des Gebarmutterkrebses. Zentralbl Gynaekol 1919;34:715-9. 3. Okabayashi H. Radical abdominal hysterectomy for cancer of the cervix uteri. Surg Gynecol Obstet 1921;33:33541. 4. Meigs JV. Carcinoma of the cervix-the Wertheim operation. Surg Gynecol Obstet 1944;78:195-8. 5. Wertheim E. The extended abdominal operation for carcinoma uteri (based on 500 operative cases). Am J Obstet Dis Women Child 1912;66: 169-232. 6. Meigs JV. Radical hysterectomy for cancer of the cervix with bilateral pelvic lymphadenectomy (the socalled Wertheim operation). In: Progress in gynecology. New York: Grune & Stratton, 1950 vol 2:540-60. 7. Peham HV, AmreichJ. Gynakologische Operationslehre. Berlin: S. Karger, 1930. 8. Okabayashi H. Abdominale systematische Panhysterektomie fur Karzinom des Uterus. Jpn J Obstet Gynecol 1928;11:136-53. 9. Kobayashi T. Abdominal radical hysterectomy with pelvic lymphadnectomy for cancer of the cervix. Tokyo: Nanzando, 1961. 10. Kobayashi T. Preservation of the pelvic parasympathetic nerves in radical hysterectomy for cancer of the cervix. In: Congress edition of the 5th World Congress of Gynecology and Obstetrics. Sandorama, September 1967: 32. 11. Yabuki Y, Asamoto A, Hoshiba T, et aI. Indication of radical hysterectomy for advanced rectal cancer. Operation 1987;42:1475-8. 12. Yabuki Y, Asamoto A, Nishimoto H, et aI. Reappraisal of cardinal ligament dissection in the Okabayashi operation for cervical cancer. In: Congress edition of the 42nd Annual Scientific Meeting of the Japan Society of Obstetrics and Gynecology. Tokyo, April 1990:345. 13. Mattingly RF. Indications, contraindications, and method of total pelvic exenteration. Oncology 1967;21 :241-59. 14. Vagi H. Extended abdominal hysterectomy with pelvic lymphadenectomy for carcinoma of the cervix. AM J 08STET GVNECOL 1955;69:33-47. 15. Nakano R. Abdominal radical hysterectomy and bilateral pelvic lymph node dissections for cancer of the cervix. Gynecol Obstet Invest 1981; 12:281-93. 16. Williams PL, Warwick R, eds. Gray's anatomy. 36th ed. Edinburgh: Churchill Livingstone, 1980. 17. Pernkopf E. Topographische Anatomie des Menschen. Zweiter Band, Berlin: Urban und Schwarzenberg, 1943. 18. Meigs JV. Radical hysterectomy with bilateral pelvic lymph node dissections. AM J 08STET GVNECOL 1951 ;62:854-70. 19. Oosterhuis JW, Lung PF, Verschueren RCJ, Oldhoff J. Viability of tumor cells in the irrigation fluid of the Cavitron Ultrasonic Surgical Aspirator (CUSA) after tumor fragmentation. Cancer 1985;56:368-70.
