Int Urogynecol J DOI 10.1007/s00192-013-2248-y

ORIGINAL ARTICLE

Cardinal ligament surgical anatomy: cardinal points at hysterectomy Andrew Samaan & Dzung Vu & Bernard T. Haylen & Kelly Tse

Received: 20 June 2013 / Accepted: 30 September 2013 # The International Urogynecological Association 2013

Abstract Introduction and hypothesis The cardinal ligament (CL) still requires more precise anatomical mapping. We aim to elucidate the anatomy of the CL and the roles it plays in gynecological surgery. Methods Studies employed sharp dissection of 28 formalinfixed cadaveric hemipelves and 10 unembalmed cadaveric hemipelves. Results The CL (total length averaging 10.0 cm) can be subdivided into three sections: a distal (cervical) section, on average 2.1 cm long, attached to the lateral aspect of the cervix (posteriorly, it was confluent with the attachment of the uterosacral [USL] ligament to form the cardinal–uterosacral confluence [CUSC]); an intermediate section, on average 3.4 cm long, running laterally (slightly posteriorly) from the cervix; a proximal (pelvic) section, relatively thick, triangularshaped on cross-section, averaging 4.6 cm long, attached to the lateral pelvic sidewall, with its apex at the first branching of the internal iliac artery. Only the distal section is free of any significant neural or vascular component (ureter is in the intermediate section) and therefore safe for surgical use. The CUSC (first pedicle of a vaginal hysterectomy and later A. Samaan : D. Vu : B. T. Haylen : K. Tse University of New South Wales, Kensington, NSW, Australia A. Samaan James Cook University, Townsville, Queensland, Australia D. Vu : B. T. Haylen University of New South Wales, Sydney, Australia K. Tse University of Sydney, Sydney, Australia B. T. Haylen (*) Suite 904, Vincent’s Clinic, 438 Victoria Street, Darlinghurst 2010, NSW, Australia e-mail: [email protected]

pedicle of an abdominal hysterectomy), if attached to the vaginal vault at hysterectomy has the potential for both lateral (CL) and supero-posterior (USL) surgical support. This pedicle would not be subsequently accessible for other surgeries. Conclusions Suggested cardinal points at hysterectomy are: know the CL anatomy; the distal section (as part of the CUSC) can provide vaginal vault support; the intermediate and proximal sections are surgically dangerous.

Keywords Cardinal ligament . Hysterectomy . Prolapse . Surgical anatomy . Vaginal vault suspension

Introduction A recent literature review [1] of the uterosacral (USL) and cardinal (CL) ligaments concluded that “section definitions and lengths and the relationship between the two ligaments needed further research”. This requirement for more precise mapping of the USL including clarity of attachments and surgically relevant points with regard to the different sections had, however, already been addressed by Vu et al. [2], expanding on earlier work by Buller et al. [3] and Campbell [4] and others. The same “more precise mapping” of the CL, yet to be performed, is the subject of the current study. As the very existence of the CL has been questioned [5, 6], confirming its presence might be a first aim. It is hoped further clarification might be given to the relationship between the USL and the CL, which together provide support for the uterus (cervix) and upper vagina [7]. Thereafter, the relevance of the CL (alone or with the USL) to the performance and safety of gynaecological surgery, in particular hysterectomy, might be assessed.

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Cardinal ligament nomenclature Kocks [8] in 1880 was the first to draw the cardinal ligament (incorrectly we would now suggest) extending from the cervix to the sacrum. In 1895, Mackenrodt [9] described a transverse cervical ligament that he named “cardinal ligament” because he hypothesised that it was the key support by virtue of its size. Subsequently, in his honour, the ligament was generally referred to as Mackenrodt’s ligament. Six more names for the same structure [1] were to be added to this before the end of the 20th century, reflecting the difficulty and lack of consensus in determining the attachments as well as the role of the CL. Even today, text books such as Hollingshead’s [10] and Gray’s anatomy [11] say the ligament is called “cardinal” because of its importance in the pelvis, without that key role being clearly stated. Ercoli et al. [12, 13] provided a morphological review of the pelvic fascia, but only a superficial glimpse of the role of each specific section of the fascia. Ashton-Miller and DeLancey [14] do address the roles of specific fascia in the pelvis with the proposed three levels of support. In this system, the CL is a level I support suspending the uterus and vagina. In 2005, Yabuki et al. [15] reasserted a German paradigm from the 1950s and further described specific relations of neurovascular structures to pelvic fasciae. Under this system, the pelvic fascia is divided into two functional groups: musculo-fascial or suspensory, e.g. USL, running in sagittal planes; and fascio-vascular or supportive, e.g. CL. Ashton-Miller and DeLancey [14] clearly stated that the CL was suspensory, yet Yabuki et al. [15] claim it is supportive. Fritsch et al. [5] in 2004 strongly asserted that first, the CL has been overinterpreted with regard to its function, and second, it is not even a supportive structure. Furthermore, in an earlier study [6], they were unable to find any structure resembling a ligament where the CL is located, leading to the recommendation that the CL should be omitted from Terminologia Anatomica. In papers supporting its existence, there has been no systematic mapping or subdivision of the CL including the total length and relative lengths of different sections. In terms of total length, the only one quoted was a mean cranio-caudal length using MRI studies [16] of 5.5–5.8 (± 1.0–1.2) cm. The published descriptions of the anatomical relationship of the CL and neighbouring USL have differed widely. Whilst some authors [3, 4] distinguished between the USL and the “so-called” (as there is the controversy over terminology) cardinal ligament (CL), others [17, 18] refer to a less defined “uterosacral-cardinal ligament complex” (UCLC). The surgical literature has noted the CL to be a dense, strong band of connective tissue. However, cadaveric and histological studies have generally demonstrated no condensed ligamentous structures [18]. Vu et al. [2] cite the CL and

USL as different ligaments becoming confluent near the edge of the cervix. Our aim is firstly to elucidate the macroscopic aspects of the CL including its total length, an appropriate division into sections (if this can be readily determined) and the relative lengths of these sections, as well as the CL proximal and distal attachments, including its relationship with the USL. We also intend to review established findings on the neurovascular relations of the CL. From this analysis, we will make anatomical conclusions relevant to gynaecological surgery, especially hysterectomy.

Materials and methods Materials The study employed sharp dissecting techniques on 28 formalin-fixed cadaveric hemipelves and 10 unembalmed cadaveric hemipelves. Institutional ethics approval was obtained. None of the cadavers had evidence of hysterectomy or pelvic floor surgery. The median age of the donors was 75. All of the cadavers were bequeathed to the Department of Anatomy, School of Medical Sciences, University of New South Wales, Sydney, Australia for scientific and teaching purposes. Morphological study of the intact CL The CLs, in embalmed and unembalmed cadavers could be made more prominent by applying very gentle traction to the uterus across the midline to the opposite side [19]. As with the USL [2], these ligaments are best seen when under a degree of tension. Observations were then made of the shape and general orientation of the intact CLs and their relations to neighbouring structures. The CLs were amenable to subdivision into three sections based on their relations with prominent landmarks, some surgically important. Measurements of the entire CL and its sections were taken with a flexible ruler to the nearest 0.01 cm. Recorded measurements were the length of the CL and the length and thickness of its sections. Terminology To avoid confusion, this report used anatomical terminology in the description of position and relations. The sacrum was described as posterior, pubic symphysis anterior. Towards the iliac crest was cranial, towards the pelvic floor caudal and towards the hip bone lateral. The portion of the CL nearer the midline was described as distal or cervical, that nearer the lateral pelvic wall proximal or pelvic.

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Dissection methods The hemipelves were dissected laterally from the median plane. Very gentle contralateral traction was applied to the uterus [2, 19] to accentuate the CL and attenuate the broad ligaments in order to define landmarks for dissection. A small incision was made along the upper (cranial) border of the broad ligament. Its anterior and posterior peritoneal layers were then peeled off its underlying connective tissue by sharp dissection. This procedure was continued caudally until the base of the broad ligament was reached where the CL began. The peritoneum was carefully dissected laterally to the lateral pelvic wall and caudally to the pelvic floor, thus exposing the entire CL. The remaining peritoneum was carefully stripped from the sacrum, rectum and uterus. The connective tissue of the CL was gradually removed to expose its vascular and neural components. The details of these neurovascular structures and their relationships with surrounding structures were noted and recorded photographically with a Nikon D80 DSLR camera with a 60-mm macro Nikkor lens.

Fig. 1 Superior view of unembalmed pelvis with uterus on traction showing the cardinal and uterosacral ligaments. The top left clamp contains the cardinal–uterosacral confluence (CUSC) and would represent the first pedicle of a vaginal hysterectomy

on the superior fascia of the levator ani, connected to it by areolar tissue. The CL also contained adipose tissue; thus, its height was variable depending on the body habitus.

Results The results will be presented in terms of general orientation and CL identification in relation to the peritoneum; CL attachments; CL sections; and CL relations to neurovascular structures. General orientation and CL identification in relation to the peritoneum When very gentle contralateral traction was applied to the body of the uterus [2, 19], two major peritoneal folds became prominent in each hemipelvis. The posterior fold running past the sides of the rectum towards the sacroiliac joints was the USL [2]. The anterior peritoneal fold extending from the lateral border of the uterus to the lateral pelvic sidewall was the broad ligament, the main part of which was the mesometrium, which extended caudally to the pelvic floor and contained the CL (Fig. 1). Removal of the peritoneum exposed a sheet of connective tissue extending laterally from the uterine body, the parametrium. At the level of the junction of the body and cervix, the parametrium was separated from the CL, in all cases, by a small “groove”, generally containing some adipose tissue. The CL presented as a prismatic band of connective tissue extending laterally (slightly posteriorly) from the lateral aspect of the cervix, broadening into its triangular attachment on the pelvic sidewall. Careful removal of connective tissue demonstrated that the apex of the triangle was found to be consistently at the point where the internal iliac artery first divided into its branches (Fig. 2). The base of the triangle rests

Attachments Distal (cervical) attachment Distally, the CL was attached to the lateral aspect of the cervix where it contributed to the pericervical fascial ring. Posteriorly, it was confluent with the attachment of the USL forming what we have termed the cardinal–uterosacral confluence (CUSC; Figs. 1, 3). This represents the first pedicle of a vaginal hysterectomy (Fig. 4) or a later/last pedicle of an abdominal hysterectomy. The CL was connected

Fig. 2 The anterior leaf of peritoneum has been retracted to demonstrate the triangular-shaped proximal attachment of the cardinal ligament (CL), the apex of which is the first division of the internal iliac artery

Int Urogynecol J Table 1 Averages and accompanying standard deviations of the cardinal ligament (CL; total and sections) in 10 unembalmed specimens Section

Length (cm)

Width (cm)

Pelvic Intermediate Cervical Total (N =10)

4.59 ± 0.60 3.41 ± 0.18 2.06 ± 0.07 10.01 ± 0.27

2.14 ± 0.16 1.77 ± 0.34 2.03 ± 0.05 N/A

the shape and contents, the CL could be subdivided into three sections: distal (cervical), intermediate and proximal (pelvic). The landmarks for this subdivision are the point of entry into (laterally) and the point of exit (medially) of the ureter from the CL (Fig. 5). The length and width of the CL and its sections have been summarised in Table 1. The height of the CL was variable. Fig. 3 A schematic diagram of the cardinal ligament (CL; dark green) and the uterosacral ligament (USL; light green) confluent distally to form the cardinal–uterosacral confluence (CUSC)

by areolar tissue caudally with the superior fascia of the levator ani and cranially with the parametrium. Proximal (pelvic) attachment The attachment of the CL on the lateral pelvic wall was a triangular area, the apex of which was the point where the internal iliac artery first divided into its branches (Fig. 2). Its posterior border usually followed the inferior gluteal artery and its anterior border the most anterior branch of the internal iliac artery. The base of the triangle lies on the levator ani. Subdivision of the CL The total length of the cardinal ligament from lateral pelvic sidewall to the cervix averaged 10.01 cm (Table 1). Based on

Fig. 4 Operative view of the first pedicle of a vaginal hysterectomy shows the CL and USL forming the CUSC

The distal (cervical) section The distal (cervical) section was very consistent in its length and structure, extending laterally from the cervix. It is also the thickest part of the CL (Table 1) owing to the formation of the CUSC. The cranial border of the cervical segment was usually clearly demarcated from the thick parametrium cranial to it by a strip of loose areolar tissue. The most prominent vascular structures related to this segment are variable distal branches of the uterine artery and a venous plexus. At the lateral end of this segment there was the division of the CUSC into the separate ligaments. The USL subsequently ran almost antero-posteriorly to form the lateral boundary of the pararectal space. The intermediate section The intermediate segment of the CL extended laterally from the separation of the USL from the CUSC (where the ureter

Fig. 5 A schematic diagram demonstrating the subdivision of the CL into sections

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exits the CL) to the point of entry of the ureter into the CL. The ureter crossed the pelvic brim at/around the bifurcation of the common iliac artery, coursed almost horizontally on the lateral pelvic wall under cover of the peritoneum before entering the CL by crossing deep to the uterine artery. In the distal (cervical) end of this section, the uterine artery was near the caudal edge of the CL, accompanied by its vein. Another uterine vein was frequently found running caudal to the ureter, separating the latter from the portion of the inferior hypogastric or pelvic plexus intervening between the CL and the levator ani. This portion of the inferior hypogastric plexus (IHP) extended from the USL to the bladder with some of its fibres reaching the uterus and vagina. The proximal (pelvic) section The proximal (pelvic) section extended from the point of entry of the ureter into the CL to the pelvic attachment of the ligament. Its thickness increased gradually and its proportion of connective tissue fibres increased as the CL coursed laterally. The ligament is relatively strong at its pelvic attachment where connective tissue was difficult to dissect off the adventitia of the branches of the internal iliac artery. The anterior portion of this section contained the major branches of the internal iliac artery, namely the internal pudendal, inferior gluteal, middle rectal, uterine, vaginal and one or more inferior vesical arteries. The deep uterine vein, when present in the proximal section, could be followed to this intermediate section and served as a useful landmark between the anterior “vascular” portion and the posterior “neural” portion of this section. Internal iliac lymph nodes were interspersed amongst the arteries. There was a variable amount of adipose tissue in this section, which was most obvious in the groove between the CL and the parametrium. In the posterior portion of this section, apart from small blood vessels, the most prominent content of the CL was a portion of the IHP or commonly referred to in surgical literature as the “pelvic plexus”, which extended anteriorly from the USL. It was located between the anterior portion of this section and the levator ani. Branches were sent from this plexus to the vagina and uterus as the plexus continued anteriorly to the bladder. Relations of the CL Relation with the ureter After crossing the common iliac artery, the ureter turned antero-medially underneath the peritoneum before entering the intermediate section of the CL. Here, it coursed medially through the anterior portion of the CL. At approximately 2 cm from the cervix, it took a sharp turn anteriorly, exited the CL and continued onwards antero-medially to enter the bladder.

Relations with neurovascular structures From anterior to posterior and cranial to caudal the CL contents were found in the following order: uterine artery, superficial uterine vein, ureter, deep uterine vein, smaller veins and most posteriorly the lateral aspect of the IHP. The deep uterine vein was a reliable landmark to determine proximity to the IHP, an important structure to avoid surgically. Given the consistent composition and interrelations of the CL, it is possible to divide it into an anterior vascular portion ending at the deep uterine vein and a posterior neural portion containing the IHP. Whilst both the proximal and intermediate sections had complex neurovascular relations, the distal section medial to the exit of the ureter, contained no important neurovascular structures.

Discussion Our studies lead us to conclude that the CL clearly exists (Figs. 1, 4) as a separate coalescence of pelvic fascia (best seen generally when under tension); its distal (cervical) section forming the CUSC with the equivalent (distal) section of the USL [2], once clearly identified, was suitable for safe surgical use; the intermediate and proximal (pelvic) sections, because of the intimate ureteric and neurovascular relations (Figs. 2, 5) should be surgically avoided. Following on from the first two conclusions, the CL might well, at times (when a macroscopic difference between CL and USL can be seen), be the predominant component of the CUSC. In Fig. 4, the CL, antero-laterally placed in the pedicle, appears bulkier than the postero-medially located USL. CL attachments and landmarks To our knowledge, this is the first paper to attempt to anatomically subdivide the CL whilst also including the interrelations of its contents and its attachments. We have noted in all specimens the attachment to the lateral pelvic sidewall as a triangular area located at the first branching of the internal iliac artery. MRI studies had suggested its origin to be near the origin of the anterior trunk of the internal iliac artery [20], though this vessel was not always visualised. The overall length of the CL at 10 cm is shorter than the USL at 12–14 cm [2]. We propose that the CL is amenable to the same sectional descriptors (distal, intermediate, proximal) as the USL [2]. The proximal attachment for the USL is the sacrum, whilst that for the CL is the pelvic sidewall. Above the CUSC, the CL runs laterally (slightly posteriorly) and anterior to the plane of the USL. Surgical support from the CL would be mainly with a vector laterally as opposed to the largely postero-superior vector of support provided by the USL [21].

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We believe the sharp dissection techniques (as described in the methodology) were a strength of the study in exposing the entire CL in all directions and limiting dissection artefact. We acknowledge that some authors [1, 16, 20, 22] have found MRI observation of the CL (and USL) very useful. However, we believe that the “more precise anatomical mapping” (as outlined in the Introduction) may have either been unachievable or technically inaccurate using MRI. Imaging should, however, play an ongoing complementary role, though not a replacement for cadaveric dissection of the CL and USL. MRI, for instance [20], has shown intermingling of the fibres of the USL and CL in the cervix and upper vagina. The current study concludes that the two ligaments become “confluent” at the cervix. Some of our results are in agreement with the previous findings of others. Range and Woodburne [19] also noted that the ureter had a pathway inside the CL at the point at which it crosses under the uterine artery. Yabuki et al. [15] also refer to the CL as having a ventral or superficial vascular part and a dorsal neural part. We have outlined the associated neurovasculature relations and we agree with part of the IHP being in the dorsal neural part [15]. Surgical relevance One reason for seeking to subdivide the CL, as previously described for the USL [2, 3], is to optimise surgical safety. In the case of the USL, it has been established that both the distal and intermediate sections are safe for surgical use [2, 3]. With the CL, we confirm that it is only the distal section that can be used and only at the time of hysterectomy. There would be no opportunity for any subsequent use of the CUSC as it would not be surgically identifiable. Such an application to gynaecological surgery is not relevant to the intermediate or proximal sections of the CL owing to the complex neurovascular and ureteric relations. The CUSC (Figs. 1, 3, 4) represents the first “pedicle” of a vaginal hysterectomy and a later/last pedicle of an abdominal hysterectomy. Vaginally, this pedicle is often attached to the vaginal vault to provide post-hysterectomy support. Similar principles are often used with (open) abdominal hysterectomy, although there is some uncertainty as to whether all laparoscopic hysterectomy techniques would necessarily employ such a principle. Our studies would strongly support this principle which provides dual level 1 [14] vaginal vault ligamentous support laterally via the CL and posterosuperiorly via the USL. Our studies confirm anatomically (what is general gynaecological surgical practice anyway) the need to carefully identify the CUSC attached to the cervix and avoid dissecting lateral to this into the CL’s intermediate section where the risks of neurovascular or ureteric injury are significant. Apart from CUSC identification at hysterectomy, complementary techniques, e.g. mobilisation of bladder and

(thus ureters) away from the cervix and CUSC, would aid surgical safety. Bilateral CUSC division, ligation and anteriorisation over the uterine isthmus (cervix partially or fully amputated) can be part of another traditional prolapse procedure, the Manchester (Fothergill) repair [23]. The distal (cervical) section of the CL, in confluence with the USL (CUSC), has surgical applications therefore in multiple traditional surgeries to provide level 1 [14] vaginal support. We would hope that our CL anatomical descriptions might assist in managing the possible hazards and morbidities from radical pelvic surgeries, particularly hysterectomy where dissection is more lateral than usual and may involve a wider dissection of the CL [24–29]. Nomenclature There has been a confusing plethora of names for what is commonly known as the CL [1]. The vast majority of authors have described the same structure albeit with minor variations in their attachments. This study demonstrated that the CL does exist and that discrepancies have been due to different paradigms of the term “ligament” and conceptions of where to delineate the fascia that makes up the CL. Based upon our results, we strongly suggest that the term CL be retained as it is a deeply entrenched term and this fascial plane is of great importance because of its contents and relations, especially so at hysterectomy. We support the removal of terms such as “uterosacral-cardinal complex” [17, 18] and particularly parametrium, which means “next to the uterus”. Cardinal points We use the definitions [30] of “cardinal” (chief, fundamental on which something hinges) and “points” to confirm (as most will be practising these already without complete anatomical clarity) some simple guidelines that might be applicable to all surgeons performing hysterectomy: know the CL anatomy; use the distal section (as part of the CUSC) for posthysterectomy vaginal vault support; and surgically avoid the intermediate and proximal sections of the CL.

Conflicts of interest None.

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Cardinal ligament surgical anatomy: cardinal points at hysterectomy.

The cardinal ligament (CL) still requires more precise anatomical mapping. We aim to elucidate the anatomy of the CL and the roles it plays in gynecol...
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