Abstract
Objective:
Radical hysterectomy/modified radical hysterectomy (RH/MRH) is one of the commonly performed pelvic surgeries. However, in most cases, bleeding is an obvious phenomenon in the zone below the uterine vessels. The current authors termed that zone in the pelvis the red alert zone. An anatomical exploration of this zone was conducted and the surgical approach was modified to learn if this would reduce the bleeding that occurs during RH/MRH.
Materials and Methods:
Two hundred and fifty-five RH/MRH operations were performed for carcinomas of the cervix, endometrium, and ovaries. The reasons for bleeding in the red alert zone were explored, and it was determined that most of the catastrophic bleeding events—such as those caused by ureteric, pelvic-nerve, and even bladder injuries—occurred inadvertently because of iatrogenic interventions by the surgeons. After the exploration, the authors modified their surgical approach for the last 105 cases. The new approach involved the following: After ligating the uterine artery and superficial uterine vein, the red alert zone of the pelvis was reached. The connective tissue of the vesicocervical ligament was divided before entering the ureteric tunnel. The ureter was freed from its attachment to the posterior leaf of the ligament. Vessels of the anterior leaf of the vesicocervical ligament were isolated, ligated, and divided. Middle and inferior vesical veins were identified, ligated, and divided in the posterior leaf of the vesicocervical ligament that was draining to the deep uterine vein. Deep cervical veins were approached similarly, safeguarding the pelvic splanchnic nerves below them.
Results:
The mean observed blood loss with the modified technique in the last 105 cases was 100 ± 50 mL, compared to 450 ± 100 mL in the cases operated on with the previous conventional technique.
Conclusions:
Anatomical knowledge is essential for reducing blood loss, as well as pelvic nerve, and ureter, and bladder injuries, during RH/MRH. (J GYNECOL SURG 36:194)
Introduction
Nerve-sparing radical hysterectomy (RH) is desirable in all indicated cases to reduce morbidity. 1 Intraoperative blood loss at a specific site makes the surgery unpleasant and complicated. The red alert zone—an area where intraoperative bleeding is likely to occur—is seen clearly by all surgeons because of this unwanted bleeding although surgeons use meticulous techniques and advanced vessel-sealing devices. This article describes the red alert zone and a safe surgical technique that can be used to lessen or avoid blood loss as well as preventing pelvic-nerve, ureter, and bladder injuries. A careful, “eagle-eyed” look at the anatomy of this zone is mandatory to prevent such complications.
Materials and Methods
Two hundred and fifty-RH/modified RH (RH/MRH) operations were performed for carcinomas of the cervix, endometrium, and ovaries. Reasons for bleeding in the red alert zone were explored, and it was determined that most of the catastrophic bleeding events—such as those caused by ureteric, pelvic-nerve, and even bladder injuries—occurred inadvertently because of interventions by the surgeons.
After the exploration, the authors modified their surgical approach for the last 105 cases. The new approach involved the following: After ligating the uterine artery and superficial uterine vein, the red alert zone of the pelvis was reached. The connective tissue of the vesicocervical ligament was divided before entering the ureteric tunnel. The ureter was freed from its attachment to the posterior leaf of the ligament. Vessels of the anterior leaf of the vesicocervical ligament were isolated, ligated, and divided. Middle and inferior vesical veins were identified, ligated, and divided in the posterior leaf of the vesicocervical ligament that was draining to the deep uterine vein. Deep cervical veins were approached similarly, while safeguarding the pelvic splanchnic nerves below them.
Results
The mean observed blood loss that occurred when the modified technique was used for the last 105 cases was 100 ± 50 mL, compared to 450 ± 100 mL in the cases operated on with the previous conventional technique.
Discussion
To gain a greater understanding of how and why the modified approach resulted in lower blood loss during these operations, it is useful to examine the pelvic anatomy in women.
The course of the ureter
In females, the close relationship of the ureter with the cervix and vagina (left > right) has clinical relevance. It is important to understand that ureter lies in the fork of the uterine vessel and the deep uterine vein.
The pelvic course
Each ureter runs retroperitoneally along the posterolateral wall of the pelvis and passes in front, just below the bifurcation of the common iliac artery at the level of ischial spine and turns medially. In males, the vas deferens crosses in front of the ureter where it is less closely related to the peritoneum. In females, the pelvic part of the ureter forms the posterior boundary of ovarian fossa. The ureter is well hidden in the tunnel formed by loose areolar tissue at the base of the broad ligament, where the ureter adheres to the posterior leaf of the ligament. The uterine artery crosses over the ureter (“water under the bridge”) ∼ 2–2.5 cm lateral to the cervix. The ureter crosses the lateral fornix of the vagina and lies close to the anterior wall of the vagina (left > right) for a short distance (∼ 1–2 cm) and then pierces the bladder wall obliquely to enter it.
The ureteric tunnel
The ureteric tunnel is a potential space between the two lips of the anterior and posterior layers of the transcervical (cardinal) ligament. The anatomy of this tunnel is the commonest site of ureteric injury during pelvic surgery (51%). 2 This tunnel contains loose areolar connective tissue, which, in turn, allows smooth (distal part) ureteric peristalsis. A blunt-tipped right-angle instrument may help elevate the roof of the tunnel as the instrument is introduced at the superior border of the ureter.
The transcervical ligament (Mackenrodt's/cardinal ligament)
This ligament extends from the supravaginal part of the cervix and the lateral part of the fornix to the lateral wall of the pelvis. This is considered the strongest ligament to support the uterus and cervix. Uterine vessels contained within the ligament.
The parametrial venous plexus
The venous plexus lies along the lateral aspect and the superior angle of the uterus within the broad ligament. The plexus extends up to the level of the cervix. Arising as paired veins, usually bilaterally, the uterine veins originate from the lateral aspect of the lower uterus adjacent to the cervix and follow the path of the uterine artery laterally, anteriorly to the ureter, and drain into the internal iliac vein within the pelvis. These are the blood vessels identified in the parametrium that have connections with the vessels of the vesicocervical ligament.
The hypogastric nerves
The superior hypogastric plexus lies in front of the sacral promontory. This plexus divides into two nerve bundles in an inverted Y fashion, and run down either side of the rectum to form the inferior hypogastric plexus behind the base of the bladder. The urinary bladder, rectum, and the internal and external genitalia are supplied by this plexus. This sympathetic hypogastric plexus also receives parasympathetic contributions from S2, S3 , and S4 and form pelvic splanchnic nerves (including both sympathetic and parasympathetic nerve fibers). The sympathetic nerves of the hypogastric plexus inhibit detrusor muscle contraction and stimulate the sphincter vesicae, thereby maintaining the bladder compliance and urinary continence. The contraction of small muscles during orgasm is also originated by these nerve fibers. The parasympathetic fibers control rectal function, detrusor contractibility, and vaginal lubrication. 3
Where injuries occur
The next step is to understand how the anatomy is connected with the most common-sites of nerve injury during pelvic surgery. These are:
In between uterosacral ligament and ureter Deep to the deep uterine vein Deep to the inferior vesical vein which runs parallel to the cervix, from posterior part of urinary bladder and paracolpium Base of the urinary bladder
The pelvic portion of the ureter has to be dissected by dividing the fascia at their medial side, as vessels supplying the ureter from the lateral side (namely, the inferior vessel artery, uterine artery, and directly from the internal iliac artery).
Why does the area below the uterine vessels comprise a red alert zone?
There are four kinds of injuries that can occur in this area? They include (1) vessels, (2) nerves, (3) ureters, and the bladder. All of these four important structures could make the surgeon and the patient unaware of injuries.
The vesicocervical ligament
The name itself suggests that this ligament is connected between the bladder and cervix. This is actually the anterior leaf of the vesicouterine ligament. In the cranial part of this ligament, the ureteric tunnel can be seen. The cranial part of the posterior leaf of this ligament lies under the ureter. This part of the ligament connects the post wall of the bladder and the lateral portions of the cervix and vagina. In the posterior leaf of this ligament, one can identify the middle vesical vein that runs from the urinary bladder (UB) to the cervix, that drains into the deep uterine vein. The inferior vesical vein runs parallel to the cervix from the post part of the UB and drains into the deep uterine vein.
Uterine veins
Each superficial uterine vein runs parallel to the uterine artery. This communication of this vein is seen at the most superficial portion of the urinary bladder and is considered to be a superficial vesical vein.
Deep uterine veins
Each side of the cervix–uterine venous plexus is there. From this plexus, each deep uterine vein runs below the ureter obliquely inferior to the uterine artery and drains into the internal iliac vein.
Pelvic surgery technique
The boundaries of the red alert zone in pelvic surgery are:
Superiorly or the base of the uterine artery and superficial uterine vein
Laterally by the ureteric tunnel and deep uterine vein
Medially by the cervix and upper vagina
Inferiorly by the base of urinary bladder.
What comprises the red alert zone?
The red alert zone is comprised of the:
Distal part of the ureter
Cervicovesical vessels and plexus
Pelvic nerves running toward the bladder
Base of the bladder.
Why the Red Alert Zone is so important for clinicians
Unexpected and unwanted blood loss in this zone is responsible for this terminology. In all types of surgical procedures—either minimally invasive or open surgery—most surgeons struggle to staunch the bleeding despite bipolar vessel sealants, and advanced energy sources and technology. In the literature, an average blood loss of 300 mL can exceed 1000 mL in this zone. 4 This is the most common site for ureteric injuries. Of four sites, 2 for hypogastric and pelvic splanchnic nerve injuries are present in this zone. These sites are deep-to-deep uterine vein and below the inferior vesicle vein, which runs parallel to the cervix from the post aspect of the bladder.
Surgical technique in the red alert zone
Up to the uterine artery, surgeons are comfortable with the dissection for RH. It is always better to ligate the uterine artery and superficial uterine vein separately. The problem starts when one enters into the red alert zone below this level.
Now the ureteric tunnel (also called the parametrial tunnel) can be seen, it is just a potential space between two layers of transcervical (cardinal) ligaments. The anterior part of this tunnel has the connective tissue of the anterior leaf of the vesicocervical ligament. Within this connective tissue, the cervicovesical vessels cross over the ureter from the posterior aspect of the bladder to the cervix. Instead of developing a ureteral tunnel, the connective tissue of the vesicouterine ligament is divided. After this division, the ureter is freed from its attachment to the posterior leaf of the ligament. Bipolar scissors or even a simple tissue-cutting scissor may help to delineate this space and to push the ureter laterally.5,6 One should avoid electrodiathermy in the vicinity of the pelvic part of the ureter.
These cervicovesical vessels should then be isolated with a blunt right angle instrument, clamped/ligated, and divided. This is easier said than done. Patience and practice are both essentially required. Then the connective tissue, within the posterior leaf of the cervicovesical ligament (bladder pillar) should be separated. In the proximal part of the posterior leaf, one can see the middle vesical vein that runs from the urinary bladder to the cervix draining into the deep uterine vein. Before this step, if one tries to ligate the deep uterine vein, there is still a chance of bleeding because of these untied tributaries, as the inferior and middle vesical veins also from the posterior portion of the bladder run parallel to the cervix and drain into deep uterine veins. The inferior vesical vein is ligated and divided. Only then, can one ligate and divide the deep uterine vein; the average blood loss is 150–200 mL. Now one could separate the bladder from the lateral part of cervix and upper vagina and hold the bladder laterally and caudally up to the cervicovesical junction, underneath it.
Blunt dissection in this area—even with bipolar electroultrasound sealant—cannot prevent bleeding in this red alert zone, as the venous plexus of the cervix, vagina, and cervicovesical vessels are resistant to surgical manipulation. They are not easy to tackle. During an attempt to control the bleeding, one tries to avoid ureter injuries. Thus, So, there is almost always considerable blood loss. The right plane is the avascular area of the anterior leaf of the vesicouterine ligament, which can prevent injury to the venous plexus. The most suitable space to separate the ureter in the ureteral tunnel is beneath the cervicovesical vessels. Figure 1 depicts the anatomical boundary of the red alert zone in an intraoperative dissection of neurovascular structures (Fig. 1A

The anatomical boundaries of the red alert zone.
Yabuki et al. 7 showed reduced blood loss and intrapelvic autonomic nerve pathways in RH, using a proper anatomical analysis of vesicouterine ligament dissection. Fujii et al. described the appropriate space to separate the ureter from the 9 o'clock position to the ureter on the right and from the 3 o'clock position to the ureter on the left craniocaudally. 8
Individual tackling of each vessel in the posterior leaf of the ligament, middle vesicle vein, inferior vesicle vein, and deep cervical vein separately leads to a less likely catastrophe.
With anatomical knowledge, it is possible to separate the ureter and the bladder from the lateral side of the cervix and the upper part of the vagina. To achieve a 2–3-cm vaginal cuff, one then separates the vagina from the bladder and rectum by cutting the paravaginal tissue (paracolpium). Care should be taken at this time to prevent damage to the pelvic nerves. Thus, one can achieve a satisfactory nerve-sparing RH. After completion of the RH, if the average blood loss is 100 ± 50 mL, that is satisfactory.
In the same way, one could identify the pelvic splanchnic nerve easily just deep to the deep uterine vein and the inferior vesicle vein. One could save the pelvic splanchnic nerves and inferior hypogastric plexus easily along with achieving a bloodless field and can prevent both bladder and ureteric injury easily in these cases.
Highlights
Visualize the anatomy of the red alert zone in the pelvis, which may also be called the Ray zone
Use magnification (2.5 × ) during dissection to identify all the structures individually
Avoid using cautery in this place; rather use a bipolar scissor or fine scissor. A cavitron ultrasonic surgical aspirator is a good option for tissue dissection
Ligate vessels individually, not together
If bleeding occurs, compress with saline soaked gauze, use fibrin sealant. and perform a traumatic suture ligation
Conclusions
Meticulous anatomical knowledge and visualization of the anatomy and deep concentration during dissection in the red alert zone is the key to reducing blood loss, nerve injuries, and bladder and ureteric injuries to perform satisfactory, nerve-sparing RHs, with either an open or a minimally invasive technique. Magnification may be used to have better vision of this zone. Patient individual vessel ligation is the key to a satisfactory outcome of this radical surgery.
Footnotes
Acknowledgments
M.D.R. and N.K. contributed equally to this work.
Author Disclosure Statement
No financial conflicts of interest exist.
Funding Information
No funding was received for this article.
