GYNECOLOGIC ONCOLOGY 00394109/01 $15.00 + .

OO

MANAGEMENT OF PELVIC
HEMORRHAGE
Rafael S. Tomacruz, MD, Robert E. Bristow, MD,
a n d F. J. Montz, MD, KM

Massive pelvic hemorrhage is a potential complication in any patient under-

going obstetric or gynecologic surgery. Intraoperative, postoperative, or postpar-
tum hemorrhage occurs predominantly as a result of unexpected vascular injury
and inability to control excessive bleeding during a surgical procedure. Knowl-
edge of the anatomic distribution of the blood supply to the pelvis and the
coagulation system, with its intrinsic and extrinsic pathways, is essential in
implementing appropriate preventive measures. Immediate recognition and
prompt action at the occurrence of pelvic hemorrhage can significantly minimize
life-threatening complications. This article reviews the management of pelvic
hemorrhage in obstetrics and gynecology, briefly discussing the blood supply to
the pelvis and the physiology of normal coagulation and focusing on the causes
and treatment of specific vascular injuries incurred during pelvic surgery.

ANATOMY

The vascular supply to the pelvis is derived predominantly from the internal
iliac (hypogastric) and ovarian arteries (Fig. 1).These vessels are connected in a
continuous arcade on the lateral borders of the vagina, uterus, and adnexa. The
ovarian arteries are direct branches of the aorta beneath the renal arteries.
They traverse bilaterally and retroperitoneally to enter the infundibulopelvic
ligaments. The hypogastric artery divides into an anterior and posterior division
and also lies retroperitoneally posterior to the ureter. The anterior division
provides the main vascular supply to the pelvis and has five visceral branches

From The Kelly Gynecologic Oncology Service, Departments of Gynecology and Obstetrics
and Oncology, The Johns Hopkins Hospital and Medical Institutions, Baltimore, Mary-
land (RST, REB, FJM); and the Gynecologic Oncology Service, Department of Obstet-
rics and Gynecology, University of the Philippines-Philippine General Hospital, Ma-
nila, Philippines (RST)

SURGICAL CLINICS OF NORTH AMERICA

- -
VOLUME 81 NUMBER 4 AUGUST 2001 925
926 TOMACRUZ et al

$' 0 Site of ligation

CIA Common iliac artery
EIA External iliac artery
HA Hypogastric artery
SGA Superior gluteal artery
sGA OA Obturator artery
SVA Superior vesical artery
UA Uterine artery
OVA Ovarian artery
IPL lnfundibulopelvic

Figure 1. Vascular supply to the pelvis and sites of ligation. (From Nelson BE, Schwartz
PE: Hemorrhage and shock. In Nichols DH, Clarke-Pearson DL [eds]:Gynecologic, Obstet-
ric, and Related Surgery, ed 2. St. Louis, Mosby, 2000, p 245; with permission.)

(uterine, superior vesical, middle hemorrhoidal, inferior hemorrhoidal, and vagi-

nal) and three parietal branches (obturator, inferior gluteal, and internal puden-
dal). The posterior division provides important collateral circulation to the pelvis
and has three branches (iliolumbar, lateral sacral, and superior gluteal). It is
important to remember that there is significant anatomic variation between
individuals in the branching pattern of the internal iliac vessels.
The female pelvis has an extensive collateral circulation that provides nu-
merous intercommunicating sources of arterial blood from various sites along
the arterial tree:
Vessels that communicate with branches from the aorta
Anastomosis of middle sacral artery with hypogastric branches
Anastomosis of lumbar and iliolumbar arteries with hypogastric branches
Anastomosis of inferior mesenteric artery with hypogastric branches
Anastomosis of superior hemorrhoidal artery with middle and inferior
hemorrhoidal arteries
Vessels that communicate with branches from the external iliac artery
Anastomosis with iliolumbar and superior gluteal arteries
 MANAGEMENT OF PELVIC HEMORRHAGE 927

Anastomosis through obturator originating anomalously from inferior epi-

gastric artery
Vessels that communicate with branches from the femoral artery
Anastomosis of deep medial and lateral femoral circumflex arteries to poste-
rior division of hypogastric artery
This vascular redundancy ensures adequate supply of nutrients and oxygen
in the unlikely event of major trauma or vascular compromise in the pelvis.
Performance of bilateral internal iliac (hypogastric) artery ligation changes the
flow characteristics from that of an arterial system to that of a venous system.
After a bilateral internal iliac artery ligation, blood supply to the major pelvic
structures is not compromised because of rerouting of blood through collateral
channels. It is imperative that the surgeon realize the importance of this collateral
circulation in evaluating and controlling hemorrhage in the pelvic area.

PHYSIOLOGY OF COAGULATION

Adequate hemostasis is the end result of all the components of the coagula-
tion system functioning together, leading to a timely and appropriate formation
and eventual dissolution of the fibrin-platelet plug. The four components of
coagulation that continuously interrelate are (1)the vasculature, (2) platelets, (3)
plasma-clotting proteins, and (4) fibrinolysis.

Vasculature

Intact vessels are endothelial-lined conduits through which red cells, white
cells, platelets, and plasma proteins freely flow. They normally inhibit coagula-
tion by the production of prostacyclin, which prevents platelet adhesion. A
disruption in the vessel wall removes the protective covering of the endothelial
cells and releases tissue thromboplastin, which activates the clotting mechanism.
The exposure of subepithelial collagen initiates platelet clumping and production
of a platelet-fibrin mass that will plug the tear in the vessel wall.

Platelets

Platelets are disk-shaped fragments of multinucleated megakaryocytes re-

leased from the bone marrow. Activation of surface receptors causes morpho-
logic changes in the platelets (changing first to a sphere and then to a spiderlike
structure with pseudopods) and the generation of thromboxane A,. These lead
to platelet aggregation and eventual formation of a platelet plug.

Plasma-Clotting Proteins

Plasma-clotting proteins are a group of serine proteases and cofactors that

interact in a synergistic system to generate fibrin. Activation of the clotting
system is initiated in two ways: the intrinsic or extrinsic pathway (Fig. 2). The
former requires no extravascular component for initiation and begins with Factor
XII, which is activated by contact with injured epithelium. The extrinsic pathway
is activated by the tissue factor thromboplastin (which subsequently activates
928 TOMACRUZ et a1

INTRINSIC PATHWAY -SIC PATHWAY I

I I

HMWK Tissue Trauma

XII

XI xla

Prothrombin ,-"bombin
VIU,PI, CA"

fibrinogen -1
Ua
Fibrin-Soluble

Figure 2. Coagulation system. HMWK = high molecular weight kallikrein; Pre-K = prekalli-
krein; K = kallikrein; PI = phospholipid.

Factor VII) when vascular disruption occurs. Prothrombin is converted to throm-

bin, which catalyzes the conversion of fibrinogen to fibrin. A clot is eventually
formed at the site of vascular injury.

Fibrinolysis

Fibrinolysis begins with the activation of the plasma substrate plasminogen.

This substrate is converted to the active enzyme plasmin, which lyses fibrin
clots and destroys fibrinogen and Factors XI1 and VII.

MANAGEMENT OF PELVIC HEMORRHAGE

Intraoperative hemorrhage during gynecologic surgery usually is encoun-

tered in the area of the infundibulopelvic ligament or ureter and the extensive
plexus of veins along the pelvic sidewall. This often occurs during difficult
intra-abdominal surgery, such as that for severe endometriosis, removal of intra-
ligamentary fibroids, or pelvic malignancies. This also may occur, although
infrequently, in the course of a simple hysterectomy for benign gynecologic
conditions. Intraoperative hemorrhage during obstetric surgery, on the other
hand, usually is encountered in cases of uterine atony, abnormal placentation,
or cervical or vaginal lacerations.
Treatment of vascular injury in the pelvis is individualized depending on
the specific vessel involved. In general, one of the most effective and rapid
methods of controlling profuse bleeding in the pelvis is by bilateral internal iliac
artery ligation. KellyIofirst performed this procedure in 1893 at the Johns Hop-
 MANAGEMENT OF PELVIC HEMORRHAGE 929

kins Hospital in an attempt to control bleeding during hysterectomy for uterine

cancer. Through the years, this procedure has been used extensively for the
initial control of severe hemorrhage within the pelvis. Bilateral uterine artery
ligation, on the other hand, has gained wide acceptance in cases of uterine
hemorrhage for various obstetric emergencies. These two methods are first
discussed separately, and the appropriate management of specific vascular inju-
ries is discussed subsequently.

Hypogastric Artery Ligation

A rapid and effective method of controlling massive pelvic hemorrhage is

through bilateral hypogastric artery ligation. There are instances during obstetric
and gynecologic surgery in which the exact location of intraperitoneal bleeding
cannot be ascertained immediately. Ligating the main source of blood supply to
the pelvis allows the surgeon to minimize the pooling of blood, granting an
opportunity to directly visualize the source of bleeding. The success rate of this
procedure in controlling uterine bleeding varies from 40% to 7, 12, 2o

Ligation of the hypogastric artery decreases the mean arterial pressure in the
downstream branches by 24%, the mean blood flow by 48%, and the pulse
pressure by 85Y0.~ Reducing blood flow allows for the identification of specific
bleeding sites, while reducing pulse pressure permits thrombosis of the bleed-
ing vessel.
The hypogastric artery is exposed by ligating and cutting the round liga-
ment and incising the pelvic sidewall peritoneum cephalad, parallel to the
infundibulopelvic ligament (Fig. 3). The ureter should be visualized and left
attached to the medial peritoneal reflection to prevent compromising its blood
supply. The common, internal, and external iliac arteries must be identified
clearly because inadvertent ligation of the common or external iliac artery results
in vascular compromise to the lower extremity. The hypogastric vein, which lies
deep and lateral to the artery, may be injured as instruments are passed beneath
the artery, resulting in massive, potentially fatal bleeding.
The hypogastric artery should be completely visualized as it branches from
the common iliac artery. A blunt-tipped, right-angle clamp (Mixter or similar) is
gently placed around the hypogastric artery, 2.5 to 3.0 cm distal to the bifurcation
of the common iliac artery. Passing the tips of the clamp from lateral to medial
under the artery is crucial in preventing injuries to the underlying hypogastric
vein (Fig. 4). Preservation of the posterior division of the hypogastric artery is
maintained with ligation at this site. After gentle mobilization of the artery by
blunt dissection, the artery is double-ligated with a nonabsorbable suture, with
the authors’ preference being 1-0 silk, but not divided (Fig. 5). The ligation is
then performed on the contralateral side in the same manner.
Complications of internal iliac artery ligation include inadvertent ligation
of the common iliac or external iliac artery, ureteral or hypogastric vein injuries,
wound infection, lower extremity paresis, and cardiac arrest.

Uterine Artery Ligation

In cases of massive uterine bleeding, bilateral ligation of the uterine arteries

may be the primary option. Fehrman8 used this method in 66 patients with
post-cesarean section hemorrhage, and only 6 patients required an emergency
hysterectomy to achieve complete hemostasis. In these situations, Fehrman be-
930 TOMACRUZ et a1

Peritoneum
overlying
iliac vessels

lnfundibulopelvic
ligament

Figure 3. Exposure of hypogastric artery. (from Nelson BE, Schwartz PE: Hemorrhage
and shock. In Nichols DH, Clarke-Pearson DL [eds]: Gynecologic, Obstetric, and Related
Surgery, ed 2. St. Louis, Mosby, 2000, p 246; with permission.)

lieves that bilateral uterine artery ligation is more effective in treating life-
threatening uterine hemorrhage compared with bilateral hypogastric artery liga-
tion.
Uterine artery ligation involves taking large purchases through the uterine
wall to ligate the artery at the cervical isthmus above the bladder flap and
adjacent to the "watershed" connecting the uterine and ovarian blood supplies
at the ovarian ligament (see Fig. 1).

LOCALES AT INCREASED RISK FOR SIGNIFICANT

VASCULAR INJURIES

Presacral Region

Massive hemorrhage occurs in the presacral region as a result of injuries to

the presacral venous plexus derived from the middle sacral veins (Fig. 6). The
presacral veins are formed not only by the lateral and medial sacral veins but
also by the basivertebral veins. These latter vessels are thin-walled, with their
adventitia blending with the sacral periosteum at the openings of their foramina.
They originate as open canals in the spongiosa of the sacral body, emerge from
their foramina, and communicate with the presacral plexus. The basivertebral
veins can be lacerated during surgery when the presacral fascia is lifted together
 MANAGEMENT OF PELVIC HEMORRHAGE 931

Figure 4. Mixter clamp gently placed around hypogastric artery from lateral to medial.
(From Nelson BE, Schwartz PE: Hemorrhage and shock. In Nichols DH, Clarke-Pearson
DL [eds]: Gynecologic, Obstetric, and Related Surgery, ed 2. St. Louis, Mosby, 2000, p
247; with permission.)

with the periosteum on the sacrum while routine lymphadenectomy is per-

formed. Because of retraction of these vessels into the bony foramina, conven-
tional measures, such as packing, cautery, suture ligation, or hypogastric artery
ligation, are often unsuccessful.
When bleeding occurs in the presacral area, immediate packing and com-
pression should be performed and maintained for 5 to 7 minutes. If bleeding
persists, two methods can be used, both of which have been proven to be
effective in providing adequate hemostasis. Metal thumbtacks can be pressed
directly over the bleeding areas in the presacral fascia and pushed all the way
into the sacrum or placed directly into each bleeding sacral foramen. The other
option is packing (occluding)the bleeding foramina with bone wax.
Bleeding in the presacral region can be avoided by dissecting superficial to
the anterior sacral artery and vein. Once the retroperitoneal space is entered, a
plane of dissection superficial to the presacral fascia and the vessels that overlie
the periosteum of the sacrum (including the basivertebral veins) is followed.
When performing a sacrocolpopexy, recognition and avoidance of the middle
sacral vessels minimizes the occurrence of this potentially fatal complication.

Obturator Fossa

The obturator artery, vein, and nerve course along the pelvic sidewall and
exit the pelvis through the obturator foramen (Fig. 7). Lymph node-bearing
932 TOMACRUZ et a1

Figure 5. The hypogastric artery is double ligated. (From Nelson BE, Schwartz PE:
Hemorrhage and shock. In Nichols DH, Clarke-Pearson DL [eds]: Gynecologic, Obstetric,
and Related Surgery, ed 2. St. Louis, Mosby, 2000, p 247; with permission.)

Figure 6. Presacral venous plexus. (From Kost ER, Mutch DG: Hemorrhage. In Baker VV,
Deppe G [eds]: Management of Perioperative Complications in Gynecology. Philadelphia,
W.B. Saunders, 1997, p 58; with permission.)
 MANAGEMENT OF PELVIC HEMORRHAGE 933

Common
iliac nodes
\
Genitofemoral
nerve External iliac
nodes
Obturator
\ I

Hypogastric / I
artery Obturator nerve, Superior
artery, vein vesical
artery

Figure 7. Major retroperitoneal vessels and their branches. (From Kilgore LC: Total Abdomi-
nal Hysterectomy with Pelvic and Paraaortic Lymphadenectomy. In Gershenson DM [ed]:
Operative Techniques in Gynecologic Surgery. 3:31-36,1998; with permission.)

tissue surrounds the obturator vessels. These vessels traverse deep to the obtura-
tor nerve, which serves as the inferior border of the traditional pelvic lymph
node dissection. Vascular injuries to the obturator artery or vein, as well as the
extensive plexus of pelvic veins located inferior to the obturator nerve, may
result in significant bleeding accompanying lymphadenectomy for gynecologic
malignancies.
Direct visualization of the obturator nerve must occur because blind and
wanton placement of suture ligatures or hemostatic clips on bleeding vessels
may result in injury to the nerve and subsequent neurologic deficits of the lower
extremity. Arterial injury is recognized easily because of the pulsatile nature of
bleeding. Ligating or clipping the obturator artery must be exact. Venous bleed-
ing may be controlled by compression with laparotomy sponges when the blood
loss is of a low rate. Suture ligation or hemostatic clips are necessary when
larger vein branches have been incised or when the flow rate (i.e., volume of
blood being lost over unit of time) is high. Further difficulties may arise when
the obturator vein has retracted into the obturator foramen, leading to a large
volume bleed into the thigh. If this occurs, the foramen, which is formed from
the fascia covering the obturator internus muscle and is not a bony structure,
may be enlarged and individual vessels clipped or ligated.
Measures to prevent vascular injuries in the obturator fossa consist of
delicate and careful removal of lymph node-bearing tissue around obturator
vessels and limiting dissection superior to the obturator nerve, thus avoiding
the plexus of pelvic veins below the nerve.
934 TOMACRUZ et al

Pelvic Floor

Vascular injuries on the so-called ”pelvic floor” are almost always inadver-
tent but may be potentially life-threatening. The major vessels involved are the
common, external, and internal iliac arteries and veins and the associated exten-
sive plexus of pelvic veins (Fig. 7). These may be injured during lymph node
dissection, difficult and extensive pelvic sidewall dissection for severe pelvic
endometriosis or cytoreductive surgery for pelvic cancers, and lateral trocar
placement in laparoscopy. Management of pelvic floor vessel injuries usually
requires rapid and effective teamwork involving the surgeon and his or her
assistants, the anesthesiologist, and the rest of the surgical-suite staff. Severe and
complex vascular injuries may require the expertise of a vascular surgeon.
Effective, timely management of vascular damage in this area is a result of
a well-executed series of actions. The surgeon’s assistant performs immediate
and gentle compression with a laparotomy sponge against the pelvic sidewall.
The anesthesiologist stabilizes the patient with administration of appropriate
fluids and blood products. Prophylactic antibiotics usually are given. Nursing
staff start preparing the special instruments that may be needed, such as vascular
clamps and fine sutures and needles. Visualization of the operative field is
optimized. Extending the abdominal incision, placing the patient in a Trendelen-
burg position with additional lateral rotation, and adjusting the laparotomy
packs to maintain the bowel away from the operative site are essential steps in
obtaining adequate visualization. One or, preferably, two suction tips are placed
adjacent to the compression pack. The surgeon performs careful and meticulous
dissection along the pathways of the injured vessel(s), inspecting the site of
injury and determining the extent and form of repair that is needed. To reiterate,
the pelvic surgeon should not hesitate in the recruitment of a vascular surgeon
for assistance. Repairs of specific injured vessels are discussed later.

Internal Iliac Vein and Pelvic Venous Plexus

Injury to the plexus of veins originating in the region of the bifurcation of
the common iliac artery and vein may result in massive catastrophic hemor-
rhage. Injuries to the internal iliac vein or its branches can occur in the course
of pelvic lymphadenectomy for gynecologic cancer staging or even during
hypogastric artery ligation. Compounding the common difficulties with manage-
ment is the relative immobility and fragility of the internal iliac vein and its
branches. The bleeding can initially be controlled with judicious pressure or
packing for at least 5 to 7 minutes. Thrombosis can occur within the smaller
branches of the internal iliac vein; bleeding in these narrow lumenal vessels
usually is effected with compression alone. However, involvement of the internal
iliac vein or the pelvic venous plexus probably will mandate further surgical
measures.
With a suction tip placed in the area of vascular injury, the pressure pack is
removed, and the surgeon identifies the site and size of the defect. A small
defect may require application of one or two hemostatic clips to close the defect.
At this point, it is essential for the surgeon to have a clear and direct visualiza-
tion of the damaged vessel before application of the clips so as to minimize
inadvertent injury to surrounding tissues or vessels. A large defect on the
internal iliac vein may be repaired with a running vascular stitch, with the
authors’ preference being 5-0 synthetic monofilament suture.
The internal iliac vein can be ligated without severe sequelae because
collateral venous drainage eventually develops between the ligated vein and the
 MANAGEMENT OF PELVIC HEMORRHAGE 935

lower extremity. To ligate the vein, vascular clamps are placed proximal and
distal to the injured structure (Fig. 8), with ligation being performed at the
proximal and distal ends using synthetic nonabsorbable suture material.
Continuous bleeding from the plexus of veins in the pelvis after compres-
sion may require intra-abdominal packing for 48 hours. Two methods, both of
which the authors have used, have been described:
1. In Masterson'sI3method, the pelvis is tightly packed with a large breast
gauze and placed into the pelvis in such a way that its removal will not
produce knots. The abdominal incision is closed with retention sutures,
leaving a 4- or 5-cm defect through which the upper part of the gauze is
brought out. Forty-eight hours later, providing that the patient is ade-
quately resuscitated and medically stable and has establishment of nor-
mal clotting and that there are no signs of further intra-abdominal bleed-
ing requiring immediate re-exploration, the patient is brought back to
the surgical suite for pack removal. The exposed portion of the gauze is
pulled, and the rest of the gauze is slowly removed. The abdominal
defect is closed with retention sutures.
2. The site of vascular injury is tightly compressed with 5-cm gauze pack-
ing, overlapped with several laparotomy packs to provide constant com-
pression around the bleeding site. The abdominal incision is closed with
retention sutures. After 48 hours, the patient is brought back to the
surgical suite, where the patient is re-explored and the pack removed.
Dkbridement of devitalized tissue, irrigation, and placement of drains
can be done. This is the "pack-and-go-back" method.21

wky DeBakev
vascula;
clamps

. . .while
%
\
&
E
s
.=
.=
. . . vein is ligated
/

Figure 8. Repair of lacerated internal iliac vein. (From Wheeless CR Jr.: Atlas of Pelvic
Surgery, ed 3. Baltimore, Williams and Wilkins, 1997, p 495; with permission.)
936 TOMACRUZ et a1

External Iliac and Common Iliac Veins

The relationships of the external and common iliac arteries to their respec-
tive veins on each side of the pelvis and abdomen are dissimilar (Fig. 9). The
right common iliac artery courses on the medial side of the common iliac vein
at its proximal portion but shifts to the lateral side of the external iliac vein as
it approaches the femoral canal. The left common and external iliac arteries
remain on the lateral side of their corresponding iliac vein throughout their
course in the abdomen and pelvis. This knowledge allows the surgeon to
anticipate potential areas of injury to the external or common iliac veins. During
lymphadenectomy for gynecologic cancer, dissection on the lateral aspects of the
left external and common iliac arteries can be performed without much risk
from injuring the underlying veins, which always maintain a medial position.
Dissection of lymph nodes on the right side, however, requires more diligence
on behalf of the surgeon, who has to delineate the borders of the iliac veins as
the iliac arteries cross from medial to lateral.
Internal iliac vein ligation, as described previously, does not compromise
the vascular function of the pelvis, but ligation of the external or common iliac
vein results in venous congestion leading to a cool, edematous, and cyanotic
lower extremity. Therefore, injuries to these veins are repaired by continuous
stitches using fine synthetic sutures and small needles.

External Iliac and Common Iliac Arteries

Although ligating the internal iliac (hypogastric) artery does not result in
ischemia to the pelvic organs thanks to the extensive collateral circulation in the
pelvis, injury to the external or common iliac arteries necessitates surgical repair

Figure 9. Anatomic relationship between common and external iliac arteries and veins.
(From Kost ER, Mutch DG: Hemorrhage. In Baker VV, Deppe G [eds]: Management of
Perioperative Complications in Gynecology. Philadelphia, W.B. Saunders, 1997, p 49; with
permission.)
 MANAGEMENT OF PELVIC HEMORRHAGE 937

because these vessels are essential conduits of blood to the lower extremity. The
external and common iliac vessels may be injured during lymph node dissection,
difficult pelvic sidewall dissection, or placement of lateral trocars during laparos-
copy. Applying vascular clamps 2 to 3 cm proximal and distal to the site of
injury (Fig. 10) initially controls hemorrhage. The arterial tear or laceration is
repaired using a continuous, monofilament polyethylene 5-0 suture placed 2 mm
from the lacerated edge with bites 2 mm apart. The proximal clamp is removed
first, permitting air, blood, and microemboli to exit through the suture line. The
distal clamp then is removed, and pulses are checked in the distal extremity.

lnfundibulopelvic Ligament

Bleeding and hematoma from the infundibulopelvic ligament usually can

be avoided by double-clamping using long, delicate clamps (Fig. 11).An initial
free tie, followed by suture ligature from proximal to distal to the cut pedicle, is
preferred. A smaller stump or pedicle containing only the ovarian vessels and
less peritoneal reflection minimizes the occurrence of loose ligature. The impor-
tance of inspection immediately after suture ligation of the pedicle and before
abdominal closure should not be underestimated.
Delayed bleeding from the transected infundibulopelvic ligament usually is
averted because suboptimal hemostasis is symptomatic intraoperatively (oozing
or spurting out of the stump or pedicle). Bleeding is usually a result of a loose
ligature around the infundibulopelvic ligament. The pedicle must be inspected
immediately after ligation of the infundibulopelvic ligament. If bleeding is found
from the stump, the pedicle is double-clamped after ensuring that the ureter is
out of harm’s way. As noted previously, the authors prefer that the initial

Figure 10. Repair of common iliac artery. (From Wheeless CR Jr.: Atlas of Pelvic Surgery,
ed 3. Baltimore, Williams and Wilkins, 1997, p 495; with permission.)
938 TOMACRUZ et al

Figure 11. Clamping, cutting, and ligating of infundibulopelvic ligament. (Modified from
Thompson JD, Warshaw J: Hysterectomy. In Rock JA, Thompson JD (eds): Te Linde’s
Operative Gynecology, ed 8. Philadelphia, Lippincott-Raven, 1997, p 805; with permission.)

ligature around the proximal clamp be a free tie, and the second tie is a
transfixion suture placed distal to the first tie through the center of the pedicle
behind the distal clamp.
Hematoma formation along the infundibulopelvic ligament is a result of
injury to the ovarian vessels secondary to crushing injuries from clamps or
leaking or rupture of a vessel following suture ligation of the cut pedicle. If
undetected or undiagnosed during surgery, hematoma formation within the
retroperitoneum can cause unexplained hypotension and anemia in the postop-
erative period. Secondary abscess formation is not an uncommon comorbidity,
converting what should have been a benign postoperative course to a life-
threatening situation.
As previously mentioned, the cut pedicle of the infundibulopelvic ligament
is inspected immediately for overt bleeding and possible hematoma formation
after it has been ligated. Prior to abdominal closure, all stumps are reinspected.
If a hematoma is found arising from the pedicle, the cut end is grasped with a
small clamp and the posterior peritoneum is incised cephalad along the course
of the ovarian vessels until the superior edge of the hematoma is reached,
guaranteeing that the ureter is identified and avoided. The top of the hematoma
can be identified by the resumption of the normal caliber of veins (narrowing)
 MANAGEMENT OF PELVIC HEMORRHAGE 939

cephalad to the hematoma. Double right-angle (Mixter) clamps are placed in

this area, again identifying and avoiding the ureter. Free tie and suture ligatures
are placed proximal to the clamps. The infundibulopelvic ligament distal to the
ligature is cut and the hematoma subsequently evacuated. Small bleeders along
the incised peritoneum are cauterized or ligated.

Aorta and Inferior Vena Cava

Injuries to the aorta and inferior vena cava (IVC) may be catastrophic
because of the massive blood loss that may follow immediately. The aorta and
IVC can be injured during lymph node dissection or midline placement of the
Veress needle or trocar during laparoscopy. Immediate exploratory laparotomy
and repair of the vessel injury are mandatory. Compression of the aorta below
the level of the renal arteries is performed to reduce hemorrhage and can be life-
saving. Vascular repair for major retroperitoneal vessels requires the expertise of
a skilled vascular surgeon.
During paraaortic lymphadenectomy, the gynecologic surgeon should
search for a small vein within the lymph node-bearing tissue anterior to the
IVC, just above the IVC bifurcation (Fig. 12). Pulling on nodal tissue in this area
can avulse the vein at its base as it enters the IVC. Knowledge of this anatomic
structure enables the surgeon to identify and clamp this small vein and avoid
vascular injury to the IVC.

Figure 12. Small vein entering the IVC within lymph node-bearing tissue. (From Kost ER,
Mutch DG: Hemorrhage. In Baker VV, Deppe G [eds]: Management of Perioperative
Complications in Gynecology. Philadelphia, W.B. Saunders, 1997, p 49; with permission.)
940 TOMACRUZ et a1

SPECIAL SITUATIONS

Laparoscopic Procedures

Vascular injuries account for 30% to 50% of surgical trauma during laparos-
copy.= The Veress needle accounts for approximately 36%, primary trocar, 32%;
and auxiliary trocar, 32% of all vascular injuries.23Bleeding can be minor and
treated with the aid of the laparoscope for abdominal wall vessel injuries or
catastrophic, requiring immediate abdominal exploration for injuries to the major
retroperitoneal vessels.

Superficial Epigastric Vessels

The superficial epigastric artery, a branch of the femoral artery that traverses
between layers of abdominal wall fascia, can be injured during insertion of
lateral trocars. Injuries to this vessel can be managed either with occlusive
pressure alone or by clamping and ligating the vessel through a small skin
incision. Transillumination of the abdominal wall with an intraperitoneal laparo-
scope may identify this artery and guide the placement of lateral trocars.

Inferior Epigastric Vessels

The inferior epigastric vessels originate from the external iliac vessels and
traverse between the rectus muscle and its posterior fascia. They are at risk for
injury during lateral placement of trocars. In contrast to superficial epigastric
vessels, these vessels are barely visualized by transillumination. The surgeon
can avoid injury to these vessels by one of the following:
Placing the auxiliary trocar in an avascular midline site
Placing the auxiliary trocar lateral to the external edge of the rectus muscle
(-= 6-7 cm lateral from the midline)
Placing the auxiliary trocar medial to the obliterated umbilical artery or
lateral to the round ligament insertion, as guided by the intraperitoneal
laparoscope
Once the injury has occurred, the sleeve should be left in place and a 20 F
catheter placed through the sleeve with a stilette (Fig. 13). After the balloon of
the catheter is intraperitoneal, the balloon is instilled with 10 mL of water and
the sleeve and catheter are both retracted, bringing the balloon taut against the
anterior abdominal wall to tamponade the injured vessel. A clamp is placed
across the catheter at the cutaneous surface to maintain tension. Another auxil-
iary trocar is replaced in a lateral position to the injured inferior epigastric
vessels. When the intraperitoneal aspect of the laparoscopy is completed, the
Foley balloon is deflated under direct visualization. Should bleeding persist, a
suture on a Keith needle is placed through the cutaneous incision, medial to the
bleeding vessel, and into the peritoneal cavity. The needle is then grasped,
inverted, and pushed through the peritoneum and rectus muscle on the other
side of the injured vessel, being brought to the anterior abdominal wall through
the aforementioned cutaneous incision. This step should be repeated to form a
figure-of-eight around the site of laceration. The suture is cut and tied, and the
site of the former bleeding is irrigated to ensure adequate hemostasis.
Often, the bleeding may not require sutures as the trocar sleeve may actually
tamponade the bleeding vessel. On completion of the laparoscopic procedure,
 MANAGEMENT OF PELVIC HEMORRHAGE 941

1 I ai:
...ha?..

...cuf t i k q flf d h e r b2edw

Figure 13. Management of lacerated inferior epigastric vessels. (From Wheeless CR Jr.:
Atlas of Pelvic Surgery, ed 3. Baltimore,Williams and Wilkins, 1997, p 377; with permission.)

the sleeve is gently removed under direct visualization and the site is observed
for bleeding. The patient is further observed in the postoperative period for
possible rebleeding and hematoma formation. Swelling, tenderness, discolor-
ation, and oozing around the trocar site with a falling hematocrit are warning
signs of abdominal wall hematoma. If this occurs, the wound is explored, the
hematoma evacuated, and bleeding vessels ligated.

Major Retroperitoneal Vessels

Exsanguination can occur following injury to major retroperitoneal vessels
(aorta, IVC, common iliac vessels) during laparoscopy. Major vessel injury has a
942 TOMACRUZ et a1

frequency of about 0.09% in general laparoscopic surgery.*Laparoscopy increases

the potential risk for these injuries. In the supine position, the patient’s umbilicus
is located directly over the lower portion of the aorta. With the patient in
Trendelenburg position, the aorta rotates upward, bringing the common iliac
vessels to the horizontal plane. The umbilicus is thus brought closer to the aorta.
Injuries to the aorta and IVC can be avoided by directing the Veress needle or
primary trocar toward the hollow of the sacrum at approximately a 45” angle
below the anterior abdominal wall fascia axis, away from the sacral promontory.
Injuries to the common iliac vessels can be avoided by directing the auxiliary
trocar downward toward the fundus of the
As mentioned previously, immediate exploratory laparotomy is performed
when injury to major retroperitoneal vessels is suspected. If the injury is caused
by placement of the Veress needle, it will be known as soon as the needle enters
the vessel if the stopcock is in the “open” position, either with a fountain of
blood if the injury is arterial, or a slower stream if the needle is placed in the
IVC or common iliac veins. If blood return is found, the stopcock should be
closed, and the Veress needle should be left in place to facilitate identification of
the bleeding site, tamponade the bleeding, and limit retroperitoneal hematoma
formation. Exploratory laparotomy through a midline infraumbilical incision is
immediately undertaken. The site of injury is identified, a 5-0 vascular polyethyl-
ene ”Z” stitch is placed above and below the site of injury, the Veress needle is
removed, and the suture is tied.

Other Areas of Intra-abdominal Bleeding

Mesosalpingeal or meso-ovarian hemorrhage also can occur from dissection,
laceration, or transection at the time of tuba1 surgery. This can be avoided by
proper selection of laparoscopic instruments and gentle handling of the fallopian
tubes and ovaries. Bleeding from this area can be controlled using bipolar
cautery, endocoagulation, hemostatic clip application, silicone band ligature,
microfibrillar collagen, or intra-abdominal sutures.
Omental or mesenteric vessels may be traumatized during trocar or Veress
needle puncture. These are best avoided by elevating the anterior abdominal
wall and directing the needle or trocar toward the pelvic area. Injury to omental
vessels may require coagulation. Mesenteric vascular injury requires closer ob-
servation because vascular compromise to the adjacent bowel may necessitate
bowel resection.

Vaginal Hysterectomy

Approximately 650,000 hysterectomies are performed annually in the United

States, 70% of which are by the abdominal r 0 ~ t e . Vaginal
l~ hysterectomies for
benign gynecologic conditions were increasingly performed over the past de-
cade, probably as a result of the rapid advancement of laparoscopy and the
marked improvement of residency training in its performance. Although it has
been established previously that abdominal hysterectomy has a higher rate of
complications in general as opposed to vaginal hysterectomy, this trend is
reversed with regard to hemorrhagic complications. The Collaborative Review
of Sterilization (CREST) Study reported an overall bleeding complication rate of
2% to 6% for vaginal hysterectomy compared with 1.6% for abdominal hysterec-
tomy9 (see Table 1).
Intraoperative hemorrhage (generally defined as loss of or requiring blood
 MANAGEMENT OF PELVIC HEMORRHAGE 943

Table 1. HEMORRHAGIC COMPLICATION RATES IN HYSTERECTOMIES

Abdominal Hysterectomy Vaginal Hysterectomy
Most Most
All Commonly All Commonly
Time of Reported Reported Crest Reported Reported Crest
Complication Rates (Yo) Rates (Yo) (%) Rates (Yo) Rates (Yo) (“h)

Intraoperative 0.2-3.7 1-2 0.2 0.5-3.5 0.7-2.5 0.7

Postoperative 0.24-2.3 1-2 1.6 0.4-5.7 1.0-5.0 1.9

transfusion of > 1 L of blood) during hysterectomy has been reported to occur

in 0.2% to 3.7% of cases.9 The CREST study reported a 0.7% prevalence of
intraoperative hemorrhage for vaginal hysterectomy compared with 0.2% for
abdominal hysterectomy. The slightly higher prevalence rate for vaginal hyster-
ectomy could be attributed to limited exposure of the operative field, leading to
more difficulty in mobilization and dissection of tissues and ligating bleeding
vessels. Conversion of vaginal hysterectomy or laparoscopic-assisted vaginal
hysterectomy (LAVH) to abdominal hysterectomy occurred in 1%to 3% or 9%
of cases, respectively.l8This surgical conversion most commonly occurs second-
ary to uncontrolled bleeding or dense adhesions.
Intraoperative bleeding during vaginal hysterectomy is usually the result of
tearing of tissues prior to clamping (from undue traction of the uterus), failure
to ligate a major blood vessel or bleeders, or slippage of ligatures. There are
certain steps during the performance of vaginal hysterectomy that require metic-
ulous attention and surgical judgment so as to prevent or minimize bleeding
complications.

Dissection of Vaginal Mucosa

1. If the initial circumferential incision is made too close to the external
cervical os, a greater amount of vaginal dissection is required prior to
entering the posterior cul de sac and vesicovaginal space (Fig. 14). It may
also be difficult finding the proper plane between the bladder and the
cervix. This disorientation is associated with a greater likelihood of in-
creased bleeding during the vaginal hysterectomy. Therefore, it is crucial
to identify the bladder reflection adjacent to the anterior vaginal wall
and make the incision just below it.
2. To minimize vascular injury, dissection in the correct cleavage plane,
preferably with the use of the Bovie to cauterize small bleeding vessels
in the vaginal mucosa, must be continued. Dissection in the incorrect
and vessel-rich plane will increase blood loss.

Uterosacral Ligament and Cardinal Ligament Ligation

1. Each uterosacral or cardinal ligament should be clamped using a single
Heaney or similar clamp. Placing two heavy Heaney clamps side-by-side
on the same ligament may cause avulsion of the pedicle. Moreover, the
lateral clamp may inadvertently injure the ureter.
2. The pedicle should be cut no more than three fourths of the way around
the tip of the clamp. Limiting this incision prevents the next pedicle
944 TOMACRUZ et a1

incision too close

Figure 14. Circumferential incision around the cervix. (Modified from Stovall TG: Hysterec-
tomy. In Berek JS (ed):Novak's Gynecology, ed 12. Baltimore, Williams and Wilkins, 1996,
p 749; with permission.)

(which may be vascular) from being cut. The authors prefer the Heaney
transfixion stitch because of the relative thickness of these pedicles.

Uterine Vessel Ligation

The uterine vessels and broad ligament peritoneum are clamped with a
single Heaney clamp and ligated with a single 1-0 or 2-0 delayed absorbable
suture. A transfixion suture should not be used on this vascular pedicle because
of the possibility of injuring a vessel and causing a broad ligament hematoma.

Utero-Ovarian Ligament Ligation

The remainder of the broad ligament and utero-ovarian ligaments are dou-
bly clamped with Heaney clamps and cut. The utero-ovarian ligaments are
double-ligated with a free ligature (to occlude the vessels in the pedicle) replac-
ing the lateral clamp, followed by a transfixion suture ligation. The double-
clamping and ligating of the utero-ovarian ligaments prevent bleeding from the
ovarian vessels.

Hemostasis
It is imperative that the surgeon visualize and inspect each pedicle for
possible bleeding. Any bleeding vessels are individually and carefully clamped
 MANAGEMENT OF PELVIC HEMORRHAGE 945

and ligated, while the surgeon ensures that the ureter and bladder have been
avoided.

Vaginal Vault Closure

Bleeding from the vaginal mucosal edges seldom occurs and, as in all cases
of abdominal hysterectomies, needs to be controlled with either a continuous
interlocking or interrupted suture. The delayed absorbable sutures are placed
through the entire thickness of the vaginal epithelium.

OBSTETRIC HEMORRHAGE

Obstetric hemorrhage is the second leading cause of maternal mortality in

the United States." In an ancient text, hemorrhage, infection, and preeclampsia
or eclampsia were described as the three apocalyptic horsemen of obstetrics.22
Obstetric hemorrhage is most often related to (1) uterine atony; (2) trauma,
vaginal or cervical lacerations, cesarean section extensions, and uterine rupture;
( 3 ) abnormal placentation, which includes placenta previa, abruptio placenta,
placenta accreta, ectopic pregnancy, and hydatidiform mole; and (4)coagula-
tion defects.
Baker3 described a classification of hemorrhage in the pregnant patient (see
Table 2). A class 1 patient is generally asymptomatic. A class 2 patient exhibits
mild tachycardia and hypotension with narrowing of the pulse pressure. A class
3 patient exhibits marked hypotension, tachycardia (120-160 bpm) and tachy-
pnea (30-50 respirations/min) with cold and clammy extremities. A patient with
class 4 presents with no appreciable blood pressure, faint peripheral pulses, and
oliguria or anuria.
Management of obstetric hemorrhage involves fluid and component replace-
ment, together with medical or surgical management. To prevent acute tubular
necrosis from massive hemorrhage, patients' urine output should be kept at
more than 30 mL/h. Moreover, maintaining a hematocrit above 30% will perpet-
uate the body's ability to handle acute blood loss.22

Nonsurgical Management

Potentially catastrophic obstetric hemorrhage is controlled by nonsurgical

means in approximately half of cases. Bleeding immediately after vaginal deliv-
ery should prompt an inspection of the vaginal vault and an assessment of
uterine tone. If uterine atony is suspected, bimanual massage of the uterus is
performed. Intravenous oxytocin (20 mIU in a 1-L fluid bottle), intramuscular
methylergonovine or prostaglandin F,, analogues (PGF,) are simultaneously

Table 2. CLASSIFICATION OF HEMORRHAGE IN THE PREGNANT PATIENT

Hemorrhage Class Acute Blood Loss (mL) Percentage Lost
900 15
1200-1500 20-25
1800-2100 30-35
2400 + 40
946 TOMACRUZ et a1

administered. In a study by Buttino and Garite? postpartum bleeding was

controlled in 85% (22 of 26) of patients receiving intramuscular PGF,. Peyser et
al” reported control of postpartum hemorrhage with continuous intrauterine
irrigation of PGE, in 22 women.
If retained placental fragments are suspected to be the cause of the uterine
atony, manual exploration of the uterus is performed. Gentle, sharp uterine
curettage is performed with specific care not to inadvertently perforate the
uterine wall.
If the estimated blood loss exceeds 1.0 to 1.5 L, blood transfusion should be
started. Historically, massive blood loss in an acute setting required transfusion
of fresh whole blood (FWB). At the present, however, blood component therapy
is preferred over FWB.
1. Packed red blood cells (PRBCs): Each unit increases hematocrit by ap-
proximately 3%; however, it is devoid of clotting factors and platelets.
2. Fresh frozen plasma (FFP):Contains fibrinogen and some clotting factors.
Each unit increases fibrinogen by 25 mg/dL. FFP generally is given in
cases complicated by disseminated intravascular coagulation (DIC).
3. Platelets: Each unit increases the platelet count by 5,000 to 10,000 cells/
mm3. If surgical intervention is anticipated, the platelet count should be
more than 50,000 cells/mm3.
4. Cryoprecipitate: Cryoprecipitate contains primarily fibrinogen, but some
clotting factors also may be present.

Surgical Management

When conservative approaches to puerperal hemorrhage fail, surgical inter-

vention must be performed. The surgical methods of controlling profuse uterine
bleeding are either vaso-occlusive (uterine, ovarian, hypogastric artery ligations)
or extirpative (hysterectomy).
Ligation of the uterine arteries is usually the primary procedure for the
control of uterine hemorrhage. OLeary and O’Leary16 described a rapid and
safe approach for bilateral uterine artery ligation. As described previously, the
uterine arteries are exposed and identified by incising the broad ligament. It is
imperative to dissect the bladder away from the cervix to displace the ureter
and prevent its injury. Two sutures (the authors’ preference being 1-0 long
lasting absorbable suture) on each side of the uterus are placed: the first at the
uterine artery insertion site and the second at the uterine artery before it
branches to the ovarian artery. Both sutures should incorporate a part of the
myometrium adjacent to the lateral border of the uterus. The reported efficacy
of this procedure is 80% to 92%.
Although there often is a drastic reduction in uterine bleeding after this
procedure, it also may be necessary to interrupt the ovarian arterial supply to
the uterus by ligating the ovarian vessels at the utero-ovarian ligament. The
blood supply to the ovaries is not compromised because ligation is performed at
the utero-ovarian ligament rather than the infundibulopelvic ligament. Bilateral
ligation of the uterine and ovarian arteries does not affect future childbearing
capacity; successful pregnancy has been reported following performance of these
procedures in a woman with postpartum hem~rrhage.’~
In 1994, AbdRabbo’ described a stepwise uterine devascularization as a
technique for management of intractable postpartum hemorrhage with preserva-
tion of the uterus. This technique utilizes five sequential steps; if bleeding is not
 MANAGEMENT OF PELVIC HEMORRHAGE 947

controlled by one step, the next step is taken until the bleeding stops, and so
on. The sequential steps are:
1. Unilateral uterine vessel ligation,
2. Contralateral uterine vessel ligation,
3. Low bilateral uterine vessel ligation,
4. Unilateral ovarian vessel ligation, and
5. Contralateral ovarian vessel ligation.
This technique was effective in controlling hemorrhage in 100% of patients.
Unilateral or bilateral uterine artery ligation alone was successful in 83% of
cases. Hysterectomy was not needed in many cases.
If ligation of the uterine and ovarian vessels is not successful in controlling
pelvic hemorrhage, bilateral hypogastric (internal iliac artery) ligation can be
attempted. As discussed in a previous section, bilateral hypogastric artery liga-
tion decreases mean blood flow by 48% and pulse pressure by 85Y0.~ This enables
the surgeon to identify particular bleeding sites and allows for intravascular
thrombosis.
If all these vaso-occlusive measures fail to control hemorrhage, a total or
supracervical hysterectomy may be the only recourse available so as to save
the woman’s life. Many gynecologist surgeons prefer to perform a subtotal
hysterectomy in these situations as less time is spent performing the procedure,
thus reducing blood loss. If a supracervical hysterectomy is performed, it must
be explicitly clear to the patient that she still has a cervix in situ and needs to
comply with recommended cervical cancer screening.

References

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Address reprint requests to

Rafael S. Tomacruz, MD
The Kelly Gynecologic Oncology Service
Departments of Gynecology and Obstetrics
Johns Hopkins Hospital and Medical Institutions
600 North Wolfe Street
Phipps 248
Baltimore, MD 21287