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Pictorial

Essay

Arterial
Anatomy
of the Female
Genital
and Relevance to Transcatheter
Embolization

Tract: Variations
of the Uterus

Jean-Pierre

Henri

Roland

Pelage12,

Olivier

ranscatheter

is

arterial

commonly

ing due

to various

causes,
disorders

[I,

arterial

2].

Recently,

uterine

arteries

of this technique

knowledge

necessitates

of the arterial

genital

tract

procedures

can

of

adjunct

anatomy

so that

safer

be performed

greater
of the fe-

of the internal

and

iliac

of its patterns of division


pictorial essay, we report
ations

in uterine

Material

Jacob3,

untargetted

studies
of

artery,

the

especially

and branches. In this


the main arterial van-

vascularization.

pictorial

study

essay

is based

on the

who

underwent

of 197 patients

embolization

between

Although

most

July
vascular

cervical

malignancies

Received

August 3, 1998; accepted

1994

and

retrospecuterine

Mourad

KardaChe1,

and

and abnormal

after revision September

nal

iliac

artery

division
uterine

and

were
artery.

Tokyo,
philic

selective

performed

nonionic

in all
contrast

Dahan1,

Jean-Pierre

Lassau2,

iohexol

(Omnipaque

France).

In six patients,

(Tracker

18;

CA) was
terization.

needed

Target

Selective

the

ipsilateral

tive

study

internal
of the uterine

using the same catheter


considerations

ity of iodinated
the

study

material

of branches

cathe-

stem
performed

Because

the potential

and radiation
of the

of

superselec-

then

in all patients.
regarding

contrast

Paris,
Fremont,

and

was

indications
for Uterine
Itely
Embolization

microcatheter

of the anterior

artery

to

of

Nycomed,

artery

was limited

in all patients.

ml of

superselective

iliac

arteries

us-

injection

Therapeutics,

study

arteries

and a hydroguidewire

a 3-French

to perform

anastomotic

Angiographic
and anatomic examinations
were
performed
by two observers
independently.
Of the
394 angiographic
studies (two each for 197 patients) that were available
for review.
19 angiograms
(5%) were excluded
because they did not
include
the internal iliac artery. Thus. 375 angio-

of the

of 10-15

300;

and other

the procedure-relevant

Terumo.

Each

consisted

artery

of the

(Radifocus:

197 patients.
media

internal

of

toxic-

exiliac

24, 1998.

Department

AJR:172, April 1999

Iioth-

anterior

origin

Japan) in 186 patients (95%)


polymer-coated
0.032-inch

des Saints-P#{232}res, 45 rue des Saints-P#{232}res, 75270 Paris

0361-803X/99/1724-989

of the
the

catheterization

catheter

Institut

AJR 1999;172:989-994

and

artery was then performed

cobra

(Radifocus)

posure,

study
to find

Superselective

uterine

and Gynecology,

or

young

healthy.
with normal
arterial
supply.
Indications
to perform
embolotherapy
were uterme myoma (n = 133); postpartum
(ii = 49), postabortion
(, = 5). and
postoperative
(n = 2)
hemorrhage:
and bleeding related to adenomyosis
(a = 3), malformation
(ii = 1 ), or cancer
(n = 4)
(Table I ). Angiography
of the contralateral
inter-

Department of Body and Vascular Imaging, H#{244}pital


Lariboisi#{232}re,
AP-HP, 2 rue Ambroise

of Obstetrics

postpartum

are usually

dAnatomie

with

bleeding

erwise

ethical

November

malformations

have complex

women

broid-related

ing a 5-French

and Methods

This

1997.

Denis

contralateral

embolization

embolization
avoided.
Angiographic
provide
a comprehensive
assessment
anatomy

the

or as

has been used in treat[3]. The widespread


ac-

leiomyoma

ceptance

trauma

embolization

to surgery

uterine

obstetric

pelvic

and

the

bleed-

including

as a preoperative

an alternative

tive

Soyer1,

vascularization,

in

of intractable

and gynecologic

male

Philippe

embolization

performed

management

ing

Le Dref1,

Rymer1

Cedex

Pare, 75475 Paris Cedex 10, France. Address

correspondence

to J.-P. Pelage.

06, France.

H#{227}pital
Lariboisi#{232}re,
75475 Paris Cedex 10, France.
American

Roentgen

Ray Society

989

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Pelage
grams of the internal iliac artery were available for
review. During the review, special attention
was
given to trunk formation and the sequence of main
branches from the internal iliac artery. The origin,
width, course, and branches of the uterine artery
were noted. Anastomoses
were searched
for. Arteries that mimicked
the uterine
artery and other
arteries selectively studied were analyzed.

three
panietal
branches
(obturator,
inferior
gluteal, and internal pudendal)
and three visceral vessels
dle rectal)
Origin

ofthe

of the uterine

(Figs.

and mid1 and 2).

division

Artery

of the uterine
oblique

the uterine
ofthe

artery

internal

artery

was usually

10 cases of life-threatening
iliac

nal

procedure
Internal

The

hemorrhage,

of the anterior

to great

on successful

in free-flow

in 191

cobra catheter

5-French

patients

the width

2). When

arteries

(26%)

used to prevent

of the uterine
(Fig.

and in-

(97%)

(1 French

2 and 5 mm. Vasospasm

the anterior

Evaluation

variation:
catheterization

tween

from

or

6).

with

artery

was

was noticed

Va.sodilators

or treat uterine

bein 97

were

artery

0.33 mm).

not

spasm.

em-

of the inter-

division

artery was preferred


and reduce radiation

was subject

artery

Thus,

iliac artery (Fig.

one, three,

from

Contralat-

artery was successful


in 97% of cases, including two different
procedures
in nine women.
In
bolization

originated

was the best projection


arose

views.

artery

four stems, ipsilateral


anterior oblique was the
best projection
(Fig. 5). The width of the uterine

jection

on anteroposterior

anterior

when
catheterization

Uterine

The origin
not visible

Superselective

uterovaginal,

(vesical,

were identified

the uterine

was based

end

Results

et al.

to shorten
exposure.

the

IliacArtery

internal

iliac

artery

terminated

into

two main stems, one anterior


and one posterior, in 77%
of cases
(Figs.
1-3).
Other
modes of division
of the internal
iliac artery
were three stems in 14%, four or more stems
in 3%,

and

main

one

stem

in 4%

of cases

4). No systematization
was possible
in
2% of cases.
In all cases, the posterior
trunk
gave rise to the iliolumbar,
the lateral sacral,
(Fig.

and the superior


superior gluteal
minal

branch.

as well defined

gluteal arteries (Fig.


artery was invariably
The

anterior

as the posterior

division

3). The

the terwas

not

stem: Usually

Fig. 2.-28-year-old
woman with primary postpartum
hemorrhage. Digital subtraction angiogram of right internal iliac artery in left anterior oblique projection
(contralateral oblique) shows division into two main
stems. Note anteriortrunk (arrow) and posterior trunk
(arrowhead).
1 = enlarged uterine artery, 2 = umbilical
artery, 3 = vaginal artery, 4 = inferior gluteal artery, 5 =
obturator artery, 6 = pudendal artery.
990

Fig. 1.-Anatomic
drawing shows lateral view of division offemale internal iliac artery into two main stems. Note
that uterine artery is branch of anterior division of internal iliac artery. Piriformis muscle (orange), sacrospinal
ligament (light green), and sacrotuberal ligament (dark green) are also portrayed.

Fig. 3.-39-year-old
woman with uterine fibroids. Digital subtraction angiogram of left internal iliac artery in
right anterior oblique projection (contralateral
oblique) shows division into two main stems. Note postenor branches: 1 = iliolumbar artery, 2 = superior sacral
artery, 3 = inferior sacral artery, 4 = superior gluteal artery. Uterine artery is indicated by arrow.

Fig. 4-41-year-old
Digital

subtraction

woman
angiogram

with uterine fibroids.


of left internal

iliac arposterior
internal puden-

tery shows division into three stems. 1


branches,
dal artery
branches.

2 = common trunk between


and inferior gluteal artery, 3 = genitourinary
Arrow indicates
uterine artery.

AJR:172, April 1999

Arterial
Course ofthe
We

Uterine

identified

Artery

the

characteristic

course of the uterine artery


of a panietal
or descending

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downward

and medially

141, which
segment

(Fig.

U-shaped
consists
running

7). a transversal

Anatomy

of the

ligament

segment

me arch

part,

segment

running

[4] (Fig.

8).

the artery

At

Female

coursing

and

Tract

the uter-

and divided

into its terminal

branches-tubal

or ascending

and ovarian-creating

anastomoses

the side

of the uterus

ovarian

[4, 5] (Figs.

angle

of the uterus,

the superior

penetrated

medially,

the marginal
along

Genital

into

the broad

ligament

branches

artery

Branches ofthe

Uterine

Most branches

with

the

9 and 10).

Artery

of the uterine

artery

were iden-

tified. The cervicovaginal


artery (Fig. I 1) was visible arising from the arch in 201 (53%) (left, 112;
tight,

89) of 375 arteries.

When

originated

from the internal

covaginal

branch

small

was not

size. Intramural

the utetine

iliac artery,
seen

branches

because
arising

artery

the ceMof its

along

the

of the uterus (also called


arcuate
arteries)
were observed in all cases (Fig. 8). The terminal
side

branches

ofthe

arcuate

with those ofthe


Ovarian

arteries

were anastomosed

contralateral

side

ofthe ovarian

artery, which arises

(Fig.

Artery

Identification
anterolaterally

from

the abdominal

the renal artery, was possible


two patients
when the catheter

sinuous

tomosed
woman with uterine fibroids. Digital subtraction
angiograms
of left internal iliac artery in
right anterior oblique projection
(contralateral)
300 oblique (A) and left anterior (homolateral)
30#{176}
oblique (B). Origin of uterine artery (arrow, A and B) is well identified on homolateral
oblique because of its upper origin.

AJR:172, April 1999

(Fig.

14). This

artery

in
at

body (Fig.
its characartery

anas-

(Figs. 9 and 10).

Arteria!Anastomoses

Fig. 5.-42-year-old

Fig. 6.-43-year-old woman with uterine fibroids treated


with gonadotropin-releasing
hormone agonists. Digital
subtraction angiogram of right internal iliac artery.
Spasm of right uterine artery (arrow) was observed before superselective catheterization was attempted.

course

with the uterine

aorta below

on aortography
was positioned

the level ofthe second lumbar vertebral


13). The ovarian artery presented
th
teristic

12).

Fig. 1.-40-year-old
subtraction

angiogram

woman with uterine fibroids. Digital


of selective

injection

into left inter-

nal iliac artery shows characteristic course of left uterine


artery panetal segment (1). arch part (2). and marginal or
ascending segment(3). Cathetershould be carefully placed
into descending segment of uterine arteryfor embolization.

Three

Transversal

types

of anastomoses
were
anastomoses
between

identified.
right and

Fig. 8.-29-year-old
woman with primary postpartum
hemorrhage related to uterine atony. Digital subtraction
angiogram

of superselective

injection

into left uterine ar-

tery shows ascending segment (1) and numerous intramural branches (2).

991

Fig. 9.-Anatomic
drawing of normal
vascularization
of uterus and adnexa shows internal iliac artery (IIA);
ovarian artery (0) originating from

left uterine
tween

the uterine

abdominal
aorta (not shown);
uterme artery (UA); uterus (U); intramural branches (IM); bladder (B); and

were

visible

in

right,

nine;

both

ment

artery

that was a branch

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cervicovaginal artery (CV). A = anastomoses between uterine and ovanan arteries.

ble in

arteries

epigastric

(10%).

Anastomoses

and ovarian

22

arteries
( 1 1%)

patients

sides,

artery

A round

seven).

embolized

be-

(Fig. 10)
(left, six;
liga-

of the proximal

was an anastomosic

to a previously

supplier
artery

uterine

in one

16).

patient(Fig.
Other

12 and 15) were visi-

(Figs.

19 patients

Procedure-Relevant

The vaginal
of the

division

Pelvic Vessels

artery

from

arising

internal

iliac

the anterior

artery

just

below

the uterine artery was identified


in 186 cases
(50%)
(left, 50; right, 32; both sides, 52) (Figs.
I

, 2, and SB). In I 8 patients


arose

artery

from

with the uterine

artery.

from the anterior

ing

division

usually

identified

in 345 (92%)

trunk

the vaginal

trunk

The vesical

iac artery
mon

(9%),

a common

above

formed

artery,

the uterine
artery

il-

artery,

of 375 cases.

with the uterine

anis-

of the internal

was

A com-

was found

in

three cases (1%) (Fig. 17). It took a downward


medial course
to reach the lateral part of the
bladder

and gave

which

were

easily

was

full (Fig.

off three

terminal

identified

when

the

branches,
bladder

l7B).

Discussion
Several

anatomy

been

have

of analysis

methods

the arterial

used

knowledge,

of variations

of the female
in previous

of cadavers

tract

To our

studies.

until now, information

dissections

gained

or during

in

genital

surgical

from

proce-

dures has been the basis of the most comprehensive accounts in the literature
[6). Angiography
has
Fig. 10-37-year-old
woman with uterine fibroids. Digital
subtraction angiogram of superselective injection of 10 ml of
iodinated-contrast
material into left uterine artery before
embolization shows anastomosis between tubal part of left
uterine artery (1) and uterine part of left ovarian artery (2).

Fig. 11.-31-year-old woman with delayed postpartum bleeding. Digital subtraction angiogram of
superselective injection into left uterine artery
shows left cervicovaginal artery (1) arising from
arch part of uterine artery (2).

been

used

formation
the origin
In our

occasionally

to

establish

trunk

of the internal iliac artery and identify


of visceral and parietal branches
[4].

series,

the relative

ofthe

ofdivision

of modes

frequencies

internal

iliac artery were differ-

ent from those previously


reported in the literature. The pattern most frequently encountered
in
our

was

study

which
than

was

division

found

the 60%

into

in 77%

two

main

stems,

of all arteries,

that was previously

more

reported

[4].

The internal iliac artery terminates


at the upper
limit of the greater sciatic notch into two main
stems,

one

anterior

and

one

posterior,

in most

cases [4]. The posterior


division
must be preserved during the embolization
of the anterior
branches

iliac artery

of the internal

rior division

of the internal

to numerous

variations.

cedures,

identification
the parietal

especially

landmarks

are

catheterization

[2]. The ante-

iliac artery

During

of these anterior
ones,

is facilitated

established
performed.

is subject
pro-

angiographic

and

branches,
if bony

superselective

Right and left symme-

try ofthe branching pattern ofthe internal iliac antery was observed in 91% of patients.
Fig. 12.-35-year-old

woman with uterine fibroids. Digital subtraction angiogram of superselective

enlarged

artery

992

left uterine

(1) and anastomosis

(2) with right uterine

artery

(not shown).

injection shows

The
division

uterine

artery

of the internal

arises

from

iliac

artery.

the

anterior

We describe

AJR:172, April 1999

Arterial

a simple

and

useful

technique

and catheterization

using

Anatomy

of the

Female

Genital

Tract

of identification

oblique

incidence:

In

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practical
terms. if the internal iliac artery is divided into two main trunks, the best projection
to identify

the origin

contralateral

anterior

inclination.
to great

The

of the uterine
oblique

width

variation;

artery

with

of the artery

enlargement

is the

20-30#{176}of
is subject

is common

in

pregnant
patients
and those with leiomyoma
[5]. In the midline,
the terminal
parts of arcuate branches of the uterine
with those of the contralateral
The

paired

ovarian

anterolateral

arteries

vides

the

dominant

ovarian

with

the uterine
blood

artery

which

arises

artery

tery,

be responsible

after

The
division

from

artery

pro-

uterus,

either

or from

in
[7].

anastomoses
branches
plays

conditions

epigastric

ing

artery

in physiologic

may

the

the renal

to the

terminal

the uterine artery [5].


The round
ligament
branch,

flow

usually

the corresponding

role

from

artery
is frequently
involved
hypervascularized
processes

the ovarian
pathologic
Each

arise

aorta below

abdominal
[7]. Although

arteries

artery anastomose
side [5].

from

of

a minor
[8].

the

This
inferior

the external
iliac arfor persistent
bleedFig. 13-27-year-old

hysterectomy.

vesical

artery

of the internal
a common

trunk

arises

from

iliac artery,
with

the anterior
sometimes

the uterine

artery,

tum hemorrhage.

pigtail catheter
teries

shows

woman with primary postparAortogram

with

5-French

located just below level of renal arovarian arteries (arrows)


sup-

enlarged

plying uterus.

Fig. 15-39-year-old
woman with polymyomatous
uterus. Gross specimen obtained after hysterectomy.
Red dye injection into left uterine artery (arrows) and blue dye injection into right uterine artery (arrowhead).
Anastomoses between both sides identified
in myometrium.

AJR:172, April 1999

obtained

Fig. 14-28-year-old
woman with numerous uterine fibroids. Digital subtraction
angiogram
of superselective
catheterization ofrightovarian
artery providing uterine vasculanzation to posterolateral intramural myoma (arrow)

shows characteristic sinuous course of ovarian artery.

woman with persistent bleeding after bilateral embolization of uterine


arteriesfor primary postpartum hemorrhage. Digital subtraction angiogram of selective injection into left external iliac artery shows left round ligament artery(1) arising from inferior
epigastric artery (2) providing blood supplyto previously embolized left uterine artery (3).
Fig. 16.-27-year-old

993

Pelage

et al.

use of a hydrophilic

polymer-coated

(rather than 0.035-inch)


vasospasm
of the uterine

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In this study
supply
edge

ofthe

0.032-inch
can prevent

guidewire
artery.

of pelvic

angiograms,

uterus is discussed.

of the normal

and variant

the blood

Precise knowlanatomy

of the

female genital tract should be the basis for accurate interpretation


of angiographic
studies
and
safe performance

of embolization

of the uterus.

References
1. Ring EJ. Athanasoulis
MN.

Baum

hemorrhage
1973;

C, Waltman AC, Margolies

S. Arteriographic

following

management

pelvic fracture.

of

Radiology

109:65-70

2. Greenwood

LH,

Glickman

MG,

Schwartz

PE,

Morse 55, Deny DE Obstetric and nonmalignant


gynecologic bleeding: treatment with angiographic
embolization. Radiology
1987:164:155-159
3. Ravina JH, Herbreteau
al. Arterial embolisation
A

Fig. 17.-41-year-old woman with uterine fibroids. Digital subtraction angiogram ofselective injection into right internal iliac artery before embolization
shows right vesical artery mimicking
course of uterine artery.
A, Selective injection into internal iliac artery shows common trunk of vesical artery (1) with uterine artery (2).
B, Superselective catheterization of vesical artery shows characteristic terminal branches (arrowheads)
allowing vesical and uterine arteries to be identified.

1995:346:671-672
4. Merland
JJ. Chiras

Merland
pelvis:

branches

of our patients.
that supply

to the bladder.
during
uterine
der necrosis,

untargeued

994

care

should

flow

be taken

to avoid
reported

bladafter

[9].

of all branches

is necessary

vesical

of the blood

embolotherapy
which has been

embolization

Identification

iliac artery
bolization

Special

It has three

80%

of the internal

to avoid untargetted
em[2, 9]. Anatomic
variants may inter-

fere with the safety

of the procedure,

high degree

to the uterus

against

offlow

unexpected

reflux

even if the

tends to protect

of the embolic

descending
segment of the uterine artery. Similarly, failure of superselective
catheterization
of
the uterine artery
lization

may lead to unilateral

and lack of therapeutic

embo-

effect [3]. The

J. Normal

JJ, Chiras J. eds.


diagnostic

and

N, et
Lancet

angiography.

Arteriographv

therapeutic

artery

Br Corn.rnrnonw
B. A composite

In:
of the

procedures.

and its branches.

1970;77:%7-975
study of the hypoga.stric
Ann Surg

7. Marx MV, Picus D, Weyman

1918;67:584-608

PJ. Percutaneous

em-

bolization of the ovarian artery in the treatment


pelvic hemorrhage. AiR 1988;150: 1337-1338

mate-

rial. To perform
safer embolization
in free-flow,
the catheter should be carefully
placed into the

to treat myomata.

Berlin: Springer-Verlag,
1981:5-68
5. Farrer-Brown
0. Beilby JO, Tarbit MH. The blood
supply to the uterus: arterial vasculature. J Obstet
Gynaecol
6. Lipshutz

as in three

D, Ciraru-Vigneron

of

8. Chait A, Moltz A, Nelson JH. The collateral


artenal circulation
in the pelvis:
an angiographic
study. AiR 1968:102:392-400
9.

Braf ZF, Koontz


plication
Urology

of

WW.

hypogastric

Gangrene
artery

of bladder:

com-

embolization.

1977;9:670-671

AJR:172, April 1999