Wo m e n ’s I m a g i n g • C o m m e n t a r y

Burbank
Pregnancy After Uterine Artery Occlusion

Women’s Imaging
Commentary
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History of Uterine Artery

Occlusion and Subsequent
W O M E N ’S
IMAGING Pregnancy
Fred Burbank1 OBJECTIVE. During mature placenta formation, select fetal trophoblasts invade ma-
ternal decidual arterioles and junctional zone arteries and change them into low-resistance
Burbank F uteroplacental arteries. Consequently, physicians performing vascular procedures that oc-
clude the uterine arteries should understand their effects on miscarriage rates, the various
toxemias of pregnancy, gross and microscopic placental anatomy, and invasive placentation.
Thus, the objective of this article is to review the effects of vascular occlusion on pregnancy.
CONCLUSION. In the long run, placental abnormalities may be the canary in the mine
shaft to globally judge the effect of uterine artery embolization on pregnancy.

Keywords: fibroids, embolization, leiomyoma, pregnancy,
uterine artery embolization
DOI:10.2214/AJR.08.2161
Received November 25, 2008; accepted after revision
November 29, 2008.
This article is a commentary on “Pregnancy After
Uterine Artery Embolization for Symptomatic Fibroids: A
Series of 15 Pregnancies” by Firouznia et al. published in
this issue of the AJR.
1
12 Old Ranch Rd., Laguna Niguel, CA 92677. Address
correspondence to F. Burbank (fburbank@cox.net).
AJR 2009; 192:1593–1600
0361–803X/09/1926–1593
© American Roentgen Ray Society
M
any authors have investigated the
effect of interrupting the blood
supply to the uterus on subsequent
pregnancy. For a woman to be-
come pregnant and experience a normal preg-
nancy after a pelvic vascular occlusion, at a
minimum, seven reproductive functions must
remain intact: ovulation; menstruation; im-
plantation and early (venous) placenta forma-
tion; mature (arterial) placenta formation; low
arterial resistance in the uteroplacental unit;
fetal nourishment; and myometrial control of
labor, delivery, and puerperal blood loss.
At least one ovary must continue to pro-
duce oocytes; enough endometrial lining
must exist to accept a blastocyst; and once
implanted, the blastocyst must develop a vas-
cular connection between mother and child.
In the first trimester, the placenta is fed pri-
marily by endometrial gland secretions and
venous blood. To develop a mature placen-
ta, one supplied by arteries, in the second
trimester select trophoblast cells of the pla-
centa must invade uterine tissues to about
the depth of the junctional zone and no fur-
ther. If invasion is shallow, an insufficient
placenta will develop. If invasion progress-
es deeper into the myometrium of the uter-
us, an invasive placenta (accreta, increta, or
percreta) will develop, the placenta will not
detach normally after childbirth, and post-
partum hemorrhage may ensue. During this
invasion, these migratory placental cells en-
gulf and enter maternal spiral arterioles and
maternal radial arteries and transform about
200 vessels into large, low-resistance utero-
placental arteries. This transformation is re-
ferred to as “physiologic change.” If enough
change does not occur in the uteroplacen-
tal arteries, resistance in the uterine arteries
will not drop, as it should, and the placenta
will be hypoxic [1–6].
A host of toxemias of pregnancy follow in-
cluding preeclampsia and eclampsia [7–13],
maternal hypertension [14], low birth weight
and short gestation length [15], and low pla-
cental volume [16]. Fetal cells must be suffi-
ciently nourished by the placenta to develop
a normal-weight baby at term. After implan-
tation, myometrium must be sufficiently in-
tact for the junctional zone and outer two
thirds of the myometrium to differentiate
into a more muscular third phenotype to in-
hibit labor until term and then, at term, ini-
tiate labor, push the baby through the birth
canal, and continue contractions for several
hours after placental delivery to slow blood
loss while clotting occurs within the uterine
vasculature as well as to redifferentiate into a
junctional zone and outer myometrium.
Menstrual history, follicle-stimulating
hormone levels, ovarian ultrasound, hyster­
oscopy, endometrial biopsy, and endometrial
ultrasound are used to assess ovulation, men-
struation, and implantation. In the end, preg-
nancy trumps all of these clinical measure-
ments and proves adequacy of these three
functions. Early placenta formation and ma-
ture placental depth can be followed up with
obstetric ultrasound or MRI. Serial obstetric

AJR:192, June 2009 1593


vital signs and clinical laboratory tests, includ-
ing soluble fms-like tyrosine kinase-1 [17–24]
and uterine artery Doppler velocitometry, re-
flect the adequacy of physiologic change of
the uteroplacental arteries. Spontaneous abor-
tion, premature delivery, or small-for-date
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babies suggest inadequate nourishment.
Throughout pregnancy, fetal nourishment
can be judged with serial obstetric ultra-
sound metrics compared with nomograms.
Placental development can be assessed by
detailed gross and histologic examination of
the placenta after delivery. Premature or in-
adequate labor and delivery and postpartum
hemorrhage each suggest abnormal myo­
metrium. An optimal investigation into the
effect of vascular occlusion on future preg-
nancy should, at a minimum, collect these
outcome variables. As we shall see, most
studies focus on only one or two of these,
primarily the ability of a woman to become
pregnant and deliver a viable baby.
Why would anyone want to occlude the
blood flow to the uterus in the first place? Ini-
tially, vascular occlusion of pelvic arteries was
performed to control bleeding during or after
childbirth. Later, occlusion therapies were de-
veloped to palliate or treat a wide variety of
pelvic disorders. This article is a review of the
effects of vascular occlusion on pregnancy.
Methods of Vascular Occlusion
Methods for occluding the blood supply to
the uterus have been around for a long time.
In a study by Kelly [25] in 1894, hysterec-
tomy, alone, was not sufficient to stop pelvic
bleeding. Ultimately, the internal iliac arter-
ies had to be ligated. However, as late as the
1940s, anatomists and clinicians still insist-
ed that after internal iliac ligation, the blad-
der and other pelvic organs would slough be-
cause of inadequate blood flow [26, 27]. In
1954, like Kelly, Hecht and Blumenthal [28]
reported the successful control of vaginal
bleeding by internal iliac ligation after hys-
terectomy. Subsequently, Sack [29] described
the successful use of the same technique to
treat massive postpartum hemorrhage in two
women after forceps deliveries. In these two
cases, pelvic bleeding was controlled with-
out hysterectomy, a large step forward in ob-
stetric care.
Because internal iliac ligation diminish-
es but does not stop blood flow in the uter-
ine arteries, direct uterine artery occlusion
evolved [27, 30–33]. In 1952, Waters [26],
in a study that was widely read around the
world, described selective uterine artery li-
1594 AJR:192, June 2009
Burbank
gation to treat postpartum hemorrhage in
eight women. He stated, “Uterine artery li-
gation will effect the same end as hyster-
ectomy, if the bleeding is from so-called
‘atony.’” He used chromic catgut as the liga-
ture material and knowingly did not divide
the uterine arteries to allow future recanali-
zation of the ligated arteries. With this tech-
nique, each main uterine artery was ligated
before its division into cervical and ascend-
ing uterine artery branches. In 1962, Alek-
sandrov [34] expanded Waters’s technique to
include bilateral uterine artery ligation and
ligation of one of the uteroovarian commu-
nicating arteries to control postpartum hem-
orrhage in two women. The technique was
further expanded to include the bilateral li-
gation of the uterine and uteroovarian com-
municating arteries to treat postpartum hem-
orrhage [35]. Tsirul’nikov [36] expanded the
technique even further with bilateral ligation
of the uterine arteries, the uteroovarian com-
municating arteries, and the arteries of the
round ligament to treat postpartum hemor-
rhage. The surgical literature showed that in
postpartum women, ligation of all visible ar-
terial input to the uterus did not damage the
uterus. Many reports of successful treatment
of postpartum hemorrhage with uterine ar-
tery ligation have been published [37–46].
In 1964 Bateman [47], a student of Wa-
ters, ligated and then resected a segment of
each uterine artery from three women who
suffered from menorrhagia. In follow-up
varying from 6 to 12 months, each woman
returned to normal menstrual cycles. Not
only was the surgical ligation and division
of the uterine arteries clinically successful,
Bateman’s work showed that in women who
were temporally distant from childbirth, the
uterine arteries could be separated from the
uterus without significant uterine damage.
In the mid-1970s, pelvic arterial embo-
lization was introduced as an alternative to
surgery to palliate pelvic bleeding caused
by malignancies [48–54]. Since then, many
have described the successful use of pelvic
artery embolization to treat a wide variety of
clinical conditions associated with vaginal
bleeding [55–73].
In 1979, in two separate articles regard-
ing the same case, Heaston et al. [74] and
Brown et al. [75] described angiographical-
ly directed pelvic arterial embolization using
“absorbable gelatin sponges” to control post-
partum hemorrhage in a 22-year-old woman
whose surgical blood loss could not be con-
trolled with the combined therapies of bilat-
eral internal iliac artery ligation, total ab-
dominal hysterectomy, and vaginal packing.
After these landmark articles, others report-
ed successful selective embolization of var-
ious pelvic arteries to control postpartum
hemorrhage [61, 63, 64, 76–101].
Uterine artery embolization (UAE) as a
treatment for women with symptomatic fi-
broids was discovered in 1995 [102, 103].
After initially using UAE to diminish blood
loss due to myomectomy, Ravina et al. [104]
later proposed UAE as a primary treatment
of women with symptomatic fibroids. After
this group’s initial small case series, UAE
was widely adopted and studied around the
world [105]. Ravina et al. believed that UAE
killed fibroids and spared myometrium be-
cause, “Physiologically, the blood flow goes
preferentially from the uterine artery toward
the peripheral myomata [fibroid arterial] net-
work. This also explains why embolization
is easy and safe if performed in a free flow,
since the particles will preferentially reach
the myomata vascular peripheral network,
thus avoiding the unwanted targets such as
the normal myometrium or ovary.” CT and
MRI studies before and after UAE and pa-
thology studies of myomectomy and hyster-
ectomy specimens after UAE support the al-
ternative view that particles injected into the
uterine arteries reach all the tissues fed by
the uterine arteries including endometrium,
myometrium, and ovaries [106, 107].
Effects of Vascular Occlusion
on Pregnancy
Fragmentary information about the effects
of each of these forms of pelvic arterial inter-
ruption on pregnancy has been published. By
1964, three successful pregnancies after bilat-
eral occlusion of the internal iliac arteries had
been reported [108, 109]. In 1969, Mengert et
al. [110] added five cases to the world’s liter-
ature; the patients in three of these cases had
bilateral ligation of the ovarian communicator
arteries as well. Over the next quarter centu-
ry, additional cases were added to the world’s
literature [111–115]. Undoubtedly, other suc-
cessful pregnancies after internal iliac liga-
tion exist; however, no systematic large-scale
study of pregnancy after internal iliac liga-
tion has been published. We know from what
has been published that women can get preg-
nant after bilateral ligation of the internal ili-
ac arteries. We do not know the pregnancy or
pregnancy complication rates.
The same limitations are true of our under-
standing of fertility after selective ligation of
 Pregnancy After Uterine Artery Occlusion
the uterine arteries. Between 1964 and 1980,
nearly two dozen full-term, successful preg-
nancies in women who had uterine artery li-
gation were published in the world’s medical
literature [38, 116–120]. From this, we can
conclude that after selective ligation of the
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uterine arteries, pregnancy is possible. How-
ever, again, we lack the pregnancy and preg-
nancy complication rates.
The world’s embolization literature is only
a bit more complete than the surgical coun-
terpart. Stancato-Pasik et al. [121] summa-
rized their experience between 1990 and
1995. During these 6 years, 17 women 20–24
years old had “gelatin sponge pledget” em-
bolization of the uterine arteries for postpar-
tum hemorrhage. Five of the 17 underwent
hysterectomy in the intervening years. Of
the 12 who did not undergo hysterectomy, 11
(91.6%) resumed menses within 2–5 months
after embolization. Three patients desired to
become pregnant and did so and delivered
healthy babies. Similarly, Deux et al. [122]
reported on pregnancy in 25 women who had
postpartum hemorrhage treated with pelvic
artery embolization between 1994 and 2000.
In this retrospective review, all women re-
sumed menstruation and one became preg-
nant. In similar chart-review studies between
1997 and 2002, Ornan et al. [95–97] iden-
tified 28 women who had pelvic artery em-
bolization for postpartum hemorrhage. Two
went on to hysterectomy. Nine women were
able to get pregnant and deliver healthy ba-
bies. Descargues et al. [123] reviewed 31
women treated with UAE for postpartum
hemorrhage. Four women went on to hyster-
ectomy. Of the 27 women who retained their
uteruses, gynecology records were available
for 25. All women returned to normal men-
ses. Of the nine patients who wanted to be-
come pregnant, five were able to conceive.
Two patients who did not want to become
pregnant did so. Of the 10 pregnancies that
occurred, four women experienced sponta-
neous abortions in the first trimester and six
carried to term, producing healthy babies.
In 2007, Gaia et al. [124] reviewed preg-
nancy after arterial embolization for the
treatment of postpartum hemorrhage in 113
consecutive patients. Of these women, 107
were available for follow-up to assess fertil-
ity, and 99 (92.5%) returned to normal men-
ses. Of these 99 women, 29 desired and at-
tempted conception, and 18 (62.1%) reported
a total of 19 pregnancies. One miscarriage
occurred at 12 weeks of gestation, whereas
18 pregnancies reached full term. Of these 18
AJR:192, June 2009 1595
women, three (16.7%) developed postpartum
hemorrhage secondary to abnormal placen-
tation. All full-term newborns were healthy.
Another group has also reported placental
abnormalities after gelatin sponge UAE for
postpartum hemorrhage [125]. Successful
pregnancy after internal iliac and uterine ar-
tery embolization for gynecologic bleeding
has also been reported by many authors [115,
126–130].
Fibroids and Fertility
Assessing the effect of vascular interven-
tions and pregnancy in women who have fi-
broids is doubly complex because it has long
been believed that fibroids themselves neg-
atively impact fertility. In a comprehensive
review of the literature, Buttram and Reiter
[131] tabulated the results from nine clini-
cal series that each evaluated the effect of fi-
broids on fertility and calculated that 27% of
women with fibroids had fertility problems.
In a review of 18 published series of pregnan-
cy rates for infertile women after myomecto-
my, the same authors calculated that 40% of
women become pregnant after myomectomy.
Furthermore, in a review of seven series that
examined the effect of fibroids on fetal wast-
age, fetal wastage decreased from 41% to
19% in women with fibroids treated with my-
omectomy [131]. However, because fibroids
are quite common, these studies certainly re-
flect some degree of coincidence. In a me-
ta-analysis of prior publications, Pritts [132]
stratified fibroids by location and showed that
fibroids had no effect on fertility if they did
not have a substantial submucosal or cavitary
component. When a submucosal or cavitary
component was present, fibroids decreased
fertility and myomectomy improved fertil-
ity. In a prospective study of 434 women re-
quiring assisted conception, Hart et al. [133]
showed that when intramural fibroids were
≤ 5 cm in diameter, pregnancy, implantation,
and ongoing pregnancy rates were reduced
by half. Even when intramural fibroids were
≤ 2.3 cm in diameter, their presence still neg-
atively influenced a woman’s odds of main-
taining an ongoing pregnancy.
In addition to decreasing fecundity, the
presence of fibroids can also complicate
a pregnancy. Qidwai et al. [134] followed
pregnancies in 15,104 women with routine
second-trimester ultrasound examinations.
Comparing the obstetric course in women
with and without fibroids, they observed that
fibroids are associated with increased risk of
cesarean delivery, breech presentation, mal-
position, preterm delivery, placenta previa,
and severe postpartum hemorrhage.
Fertility After UAE for the
Treatment of Symptomatic Fibroids
Because a large number of UAE proce-
dures for fibroid treatment have been per-
formed worldwide, considerable information
is available about pregnancy after UAE. Only
3 years after the original publication by Rav-
ina et al. [103], this group reported that seven
pregnancies occurred in their treatment popu-
lation [135]. Five of the seven women were
over 38 years and two were below 30 years of
age. One woman experienced a miscarriage,
and a woman with AIDS delivered prema-
turely. Five additional pregnancies were lat-
er reported from the same group [136, 137].
McLucas et al. [138] reported pregnancy in-
formation after UAE in 400 women, 139 of
whom wished to remain fertile after UAE.
Seventeen pregnancies occurred, with 10 nor-
mal deliveries. Five women aborted spontane-
ously, and two were still pregnant at the time
of publication. Many additional case reports
and clinical series describing pregnancy after
UAE have appeared [139–146]. One case re-
port described spontaneous twins in a 29-year-
old woman after UAE [147]. Recently, Pinto
Pabón et al. [148] followed 57 women who
wanted to become pregnant in a series of 100
women treated with UAE for symptomatic fi-
broids. Eleven (19.3%) pregnancies were ob-
served in these 57 women, resulting in eight
live births. Early miscarriages occurred in
three (27.3%) of these 11 women. No abnor-
mal placentation was observed.
Clearly, it is possible for a woman to be-
come pregnant and deliver a healthy baby
after UAE treatment of fibroids. The ques-
tions then become, at what frequency does
pregnancy occur and how normal are these
pregnancies? Pregnancy rates vary consider-
ably. Gaia et al. [124] reported pregnancy in
18 (62.1%) of 29 women seeking pregnancy.
Honda et al. [149] reported that five (50%) of
10 women seeking pregnancy conceived af-
ter UAE. On the other hand, Pinto Pabón et
al. [148] reported a rate of only 19.3%.
A comprehensive report of pregnancy after
UAE came from the Ontario Uterine Fibroid
Embolization Trial [150–152]. In this trial,
555 women underwent UAE. The average pa-
tient age was 43 years with a range from 18 to
59 years. Twenty-two women conceived,
three twice, for a total of 25 pregnancies. Four
spontaneous and two elective abortions were
observed. Eighteen live births were reported.

Fourteen were at term and four were pre-
term. Nine women delivered vaginally and
nine by cesarean delivery. Four newborns
were small for gestational age. None of these
statistics should raise eyebrows given that
they come from a population of mothers with
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fibroids and an average age of 43 years. How-
ever, placentation abnormalities, which are
rarely seen, were observed at a very high
rate: three (16.7%) of the 18 pregnancies.
Two cases of placenta previa, one of which
was a placenta accreta and the other placenta
accreta that required cesarean hysterectomy,
were identified. All three women with pla-
cental abnormalities were nulliparous, which
makes these findings of even greater con-
cern. Additionally, two (3.4%) of 18 preg-
nancies were complicated by gestational hy-
pertension, which may have been secondary
to a placentation abnormality as well.
To better understand the effect of UAE on
pregnancy, Goldberg et al. [153] performed a
systematic literature search comparing UAE
to myomectomy. They examined published
materials and contacted authors for addition-
al data to compare 53 pregnancies after UAE
with 139 after myomectomy. From this retro-
spective search (which included patient demo-
graphics, fibroid characteristics, and pregnan-
cy complications), they showed that women
who had UAE were significantly older, higher
in parity, and had larger fibroids than women
treated with myomectomy (all three differenc-
es significant at p ≤ 0.001). Consequently, the
two patient populations that the authors want-
ed to compare were not comparable. Despite
this bias in favor of myomectomy (young-
er women with smaller fibroids), no statisti-
cally significant difference was observed in
the rate of spontaneous abortion, postpartum
hemorrhage, cesarean delivery, or small-for-
gestational-age babies. At the p ≤ 0.05 level,
preterm delivery and malpresentation were
observed more commonly in the UAE group
(16% vs 3% and 11% vs 3%, respectively).
Because the UAE women were older and had
larger fibroids, a difference of this magnitude
would not be surprising.
In 2008, Holub et al. [154] reported a pro-
spective, randomized comparison of the im-
pact of UAE and myomectomy on pregnan-
cy. One hundred twenty-two women who
presented with intramural fibroids > 4 cm
and who wanted to become pregnant were
randomly assigned to either UAE or my-
omectomy. The rate of technical success,
symptomatic effectiveness, postprocedural
follicle-stimulating hormone levels, number
1596 AJR:192, June 2009
Burbank
of reintervention procedures for fibroid re-
currence or regrowth, and complication rates
were no different between the two proce-
dures. Forty women after myomectomy and
26 after UAE had tried to conceive. More
pregnancies (n = 33) and labors (n = 19) and
fewer abortions (n = 6) were observed after
myomectomy than after embolization (17
pregnancies, five labors, and nine abortions;
differences statistically significant at the p <
0.05 level). The authors concluded that myo-
mectomy led to, “superior reproductive out-
comes in the first 2 years after treatment.”
Holub et al. [154] prospectively compared
the effect on pregnancy of surgical occlusion
of the uterine arteries in 38 women to UAE
in 20 women who conceived after fibroid
treatment. When the uterine arteries are oc-
cluded surgically, no embolic particles are
present in the arteries and arterioles of the
uterus. Pregnancies after UAE had a higher
rate of spontaneous abortion (56%) than did
pregnancies after surgical uterine artery oc-
clusion (10.5%). The authors concluded that
after UAE, pregnancies had “significantly
increased risk for spontaneous abortion.”
Conclusion
With respect to the seven reproductive
functions introduced at the beginning of this
article, how many did Firouznia et al. [155]
evaluate in “Pregnancy After Uterine Artery
Embolization for Symptomatic Fibroids: A
Series of 15 Pregnancies”? Menstrual histo-
ries after UAE were not reported. What we
do know is that the crude pregnancy rate in
this relatively young population of women
with symptomatic fibroids (mean age, 32.3
years) was high at 60.9%. One baby was
small for gestational age. One postpartum
hemorrhage was observed, although the rea-
son for the postpartum hemorrhage was not
established. Was it atony related to myome-
trial inadequacy, was it an invasive placenta,
or was it related to the surgical delivery? The
toxemias of pregnancy are not mentioned in
this article. Did none occur? Two spontane-
ous abortions were recorded. No woman was
allowed to deliver vaginally, so information
about myometrial adequacy is unknown. Be-
cause the data for this study were obtained
from “physician’s offices and hospitals,” de-
tailed pathologic examination of each pla-
centa, unfortunately, was not available.
Given how the arterial placenta forms, we
would expect to observe that embolic parti-
cles located in and around uterine arterioles
and arteries might present a biologic dilem-
ma to migrating fetal trophoblasts. Fetal tro-
phoblasts have evolved to transform normal
maternal decidual arterioles and junctional
zone arteries into low-resistance uteropla-
cental arteries. Evolution has not prepared
these migratory cells to bump into and,
somehow, deal with plastic particles attached
to the walls of uterine arteries. Consequent-
ly, in addition to pregnancy rates and birth
weights, understanding the effects of inter-
rupting the blood supply to the uterus should
also include a focus on early spontaneous
abortion, the various toxemias of pregnancy,
gross and microscopic placental anatomy,
and invasive placentation. In the long run,
placental abnormalities may be the canary in
the mine shaft for globally judging the effect
of UAE on pregnancy.
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F O R YO U R I N F O R M AT I O N
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appears on the preceding pages.
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