1025022

review-article2021
JETXXX10.1177/15266028211025022Journal of Endovascular TherapyHoang et al

A SAGE Publication

Review

Journal of Endovascular Therapy

Uterine Arteriovenous Malformation:

1­–17
© The Author(s) 2021
Article reuse guidelines:
A Pictorial Review of Diagnosis and sagepub.com/journals-permissions
DOI: 10.1177/15266028211025022
https://doi.org/10.1177/15266028211025022

Management www.jevt.org

Van Trung Hoang1 , Hoang Anh Thi Van1, Cong Thao Trinh2,
Ngoc Trinh Thi Pham3, Chinh Huynh4, To Nguyen Ha4, Phuong Hai Huynh5,
Hoang Quan Nguyen6, Uyen Giao Vo7, and Thanh Thao Nguyen8

Abstract
Uterine arteriovenous malformation (UAVM) is a rare condition and is classified as either congenital or acquired UAVM.
Patients with UAVMs usually experience miscarriages or recurrent menorrhagia. Ultrasound is used for the initial estimation
of UAVMs. Computed tomography and magnetic resonance imaging are noninvasive and valuable methods that provide
good compatibility with digital subtraction angiography to support the diagnosis and treatment of UAVM. Timely diagnosis
is crucial to provide appropriate treatment for alleviating complications. This article presents a pictorial and literature
review of the current evidence of the diagnosis and management of UAVM.

Keywords
angiography, duplex ultrasound, magnetic resonance angiography, uterine arteriovenous malformation, vascular anomalies,
vascular malformation

Introduction
Uterine arteriovenous malformation (UAVM) is a rare con- 1
Department of Radiology, Thien Hanh Hospital, Buon Ma Thuot,
dition that may cause vaginal hemorrhage and possibly lead Vietnam
to a life-threatening state.1 UAVM was first described by 2
Department of Radiology, Hue Central Hospital, Hue, Vietnam
3
Dubreuil and Loubat in 1926.2 It is classified as a congenital School of Medicine and Pharmacy, The University of Danang, Vietnam
4
Department of Radiology, Tu Du Hospital, Ho Chi Minh City, Vietnam
or acquired type and the latter accounts for the majority of 5
Department of Radiology, University Medical Center at Ho Chi Minh
cases.3 City, Vietnam
UAVMs are unnatural connections among uterine arteries 6
Department of Radiology, Da Nang Oncology Hospital, Da Nang,
and veins (Figure 1), which usually occur during fertile age.4 Vietnam
7
It is a dilatation of vessels in alternating space deep inside Department of Vascular Surgery, Fiona Stanley Hospital, Murdoch,
Western Australia, Australia
the myometrium, with the absence of the capillary vessels, 8
Department of Radiology, Hue University of Medicine and Pharmacy,
letting a direct flow from the arterial system toward the Hue University, Hue, Vietnam
venous system.5 UAVMs can be categorized as high-flow
Corresponding Authors:
vascular malformations, and signified by a high-pressure Van Trung Hoang, Department of Radiology, Thien Hanh Hospital, 17
gradient across the arterial and venous system, that enables a Nguyen Chi Thanh Street, Buon Ma Thuot, 630000, Vietnam.
high vascular flow through the nidus. The central nidus is Email: [email protected]
defined as a tangle of vessels in which often multiple arteries Ngoc Trinh Thi Pham, School of Medicine and Pharmacy, The University
and veins converge.6 Currently, AVMs are classified based of Danang, 41 Le Duan Street, Da Nang 550000, Vietnam.
on the Yakes AVM classification system, which helps guide Email: [email protected]
the treatment strategy (Figure 2).7 “Uterine vascular malfor- Thanh Thao Nguyen, Department of Radiology, Hue University of
mation” is diagnosed when a lesion detected with ahyper- Medicine and Pharmacy, Hue University, 06 Ngo Quyen Street, Hue
vascular and turbulent flow.8,9 The term UAVM should be 530000, Vietnam.
moderated to those lesions showing a hypervascular mass Emails: [email protected], [email protected]
2 Journal of Endovascular Therapy 00(0)

Figure 1. Illustration of a uterine arteriovenous malformation (UAVM) lesion. UAVMs are classified as congenital and acquired.2–4

Figure 2. Schematic drawing of the Yakes classification of arteriovenous malformations (AVMs). Red represents arteries and
arterioles, purple represents the mixing of arterial and venous blood, blue represents veins.7
Hoang et al 3

with early filling on angiography or pathologic examination Epidemiology

of the uterus after hysterectomy.8–10
The clinical significance of UAVMs is mainly related to The true incidence and prevalence of UAVMs are difficult
their potential life-threatening bleeding and the extreme chal- to determine because of their scarcity. Furthermore, many
lenge of emergent diagnosis and management once this hap- cases in which UAVM had responded to medical treatment-
pens. UAVM is also a cause of recurrent miscarriages if not might have been missed. Several studies prospectively
well controlled.1,6,10 Furthermore, this rare entity has received evaluate the incidence of uterine vascular malformations,
much attention in the literature but is poorly understood, including UAVMs, developing after abortion or delivery by
especially in terms of advanced imaging diagnosis, molecu- using transvaginal color Doppler ultrasound (US).18,19
lar medicine, and multimodal management combinations. There is little information about the frequency of these
lesions in the literature. UAVMs make up about 1% to 2%
of all genital and intraperitoneal hemorrhages.20 Less than
Materials and Methods 150 cases of UAVM have been reported in the literature
As the aim of this review was to provide a knowledge since the first documented observation in 1926 by Dubreuil
update to supplement the current literature, a narrative and Loubat, and just 73 cases reported before 1997.12,21–23
review was conducted on clinical presentation, investiga- In a study ofHiroyuki Yazawa including 959 patients, 1
tions, and management of UAVM. A literature search was patient was diagnosed with UAVMs using transvaginal
performed in PubMed and Google Scholar to identify and US.24 O’Brien et al25 identified a primary incidence of
evaluate all articles related to UAVM published from UAVMs as 4.5% (21 of 464 patients) through transpelvic
February 1926 up to January 2021. The search terms were US exams for uterine bleeding. Because of the increased
words related to UAVM, such as “uterine AVM,” “uterine use of US, UAVMs are being diagnosed with increased
arteriovenous malformation,” “diagnosis of uterine arterio- frequency.26
venous malformation,” “treatment and management of uter-
ine arteriovenous malformation,” and “uterine arteriovenous Histopathology
malformation intervention.” Besides, the search is then
expanded to search terms as “AVM,” “arteriovenous mal- Histopathology of UAVM is diverse and is often investi-
formation,” “pelvic arteriovenous malformation,” “pelvic gated if a patient has had surgery or a hysterectomy.Common
arteriovenous fistulas,” “vascular pathology of the uterus,” pathological features include the presence of multiple vascu-
“imaging of AVM,” and “diagnosis and management of lar fibrous nodules including veins and arteries.23,27 They
AVM.” Reference lists of selected articles were also appear diffusely to the entire uterine wall from the serosa to
searched. The categories of articles taken into review the endometrium. The arrangement of vascular structures is
include original researches, reviews, reports, opinions, and branched, plicated with diversified size, and many fibrous
communications. In addition, we also compiled a series of follicles. Many thick-walled blood vessels are discovered to
diagnostic and managing imaging of UAVM. be blocked in the uterine muscle.17,22,23,28 Lesions manifest
with diffuse, well-delimited, and well-distinguished cells
without abnormal cells at the endothelium.29–31 In cases of
Etiology detecting after embolization, a circular localized lesion rep-
UAVMs can be congenital or acquired. Congenital UAVM resenting intravascular embolism is often observed.32–34 In
is believed to arise from an arrest or failure of embryologic addition, the presence of necrotic membranes may be con-
differentiation in the primitive capillary plexus, resulting in sidered a risk factor for UAVM associated with the recent
anomalous speciation in the capillaries and abnormal com- pregnancy of the patient.9,35,36
munication among arteries and veins.11,12 Congenital
UAVMs tend to have multiple feeding arteries, a central
nidus, and numerous large draining veins, so it typically
Genesis of UAVM
enlarges over the uterus and invades into the surrounding Recent studies revealed mutation of the RASA-1 gene on
pelvis.13,14 Acquired UAVM, on the other hand, is resulted 5q13-22 is responsible for many congenital capillary mal-
from prior uterine interventions such as pelvic surgery, ther- formations and AVMs).37–39 Heterogeneity in phenotype
apeutic abortion, curettage procedures, or cesarean sec- and slightly decreased penetration capacity indicated that a
tion.15 It can be associatedwith infection, a retained product double-hit mechanism was associated with lesion forma-
of conception, gestational trophoblastic disease, cervix or tion.40,41 The Ras/MAP kinase pathway is negatively modu-
endometrial cancer, malignancy and exposure to diethylstil- lated by p120RasGAP. When activating the receptor
boestrol, and direct uterine trauma, which occur more fre- tyrosine kinase, it is individually enlisted to the plasma
quently in women at reproductive age.3,16 Another membrane, or by Annexin A6, to inactivate Ras.42 It also
suggestion of a cause of acquired UAVM is the association associates with p190RhoGAP to rule cell mobility and is
of necrotic villi in the venous sinuses of scar tissues.9,17 linked to AKT to keep cells away from apoptosis.43
4 Journal of Endovascular Therapy 00(0)

Table 1. Common Imaging Findings of Uterine Arteriovenous Malformation (UAVM).2,19,25,54–62

Methods Findings
General features A bulky uterus and vague mass lesion with penetration of adjacent tissues. These lesions have very
little mass effect with soft tissue spaces. Dilated, zigzag feeding arteries, and enlarged draining
veins with central nidus. Flows have high velocity and early enhancement of lesions. There may
be hemorrhage, thrombosis, or calcification. In acquired UAVM, the typical abnormality is the
connection between an artery and a vein, meanwhile, congenital UAVM usually associates with
multiple arteries and veins.
Grayscale ultrasoundS The grayscale unlrasound shows subtle myometrial heterogeneity or has small anechoic spaces in
the myometrium. Thickening uterine muscle with mixed echogenic areas and the multiple tubular
or spongy anechoic or hypoechoic areas within the myometrium may present. Mixed echogenic
mass in the uterus may be mistaken with retained products of conception.
Color Doppler Nonspecific hypoechoic nodules, mosaic uterine color flow pattern. Ultrasound reveals intense
vascularity with the chaotic, omnidirectional flow. These areas consist of curving vessels with
patterns of the various orientation of color flow.
Spectral Doppler The arterial channels show low pulsatility and the venous waveforms show pulsatile and high-
velocity flow. Lesions have high peak velocity (mean peak systolic velocity = 136 cm/s) and low
resistance (mean resistance index = 0.3) flow.
Computed tomography Computed tomography allows observation of multiple dilated feeding arteries, enlarged draining
veins, and central nidus, although it is often difficult to distinguish closely adjacent vessel channels.
Occasionally aneurysms or varicose veins can be observed. Other features include thickening and
enlargement of adjacent structures as interstitial tissue, fat, muscles, and bones. Complications
such as hemorrhage and the presence of calcification, thrombosis, or combined lesions.
Computed tomography angiography also allows the assessment flow of lesions.
Magnetic resonance imaging Magnetic resonance imaging findings comprise a bulky uterus, vague mass, focal or diffuse
disruption of the junctional zone. Lesions presence of multiple circuitous and serpiginous flow-
related signal voids in the myometrium and parametrium. The feeding artery and the draining vein
are almost always seen. When UAVMs jut into the endometrial cavity, they may have a polypoid
shape.
Digital subtraction angiography The immediate opacification filling of many enlarged veins from a nidus fed by bilateral
hypertrophic uterine arteries. On digital subtraction angiography, it is possible to intervene to
block UAVM lesion with embolized materials.

Identifying the participation of RASA1 gives rise to the UAVM.9,51,52 Findings on physical examination such as pal-
evolution of novel therapeutic approaches that help distin- pation of abnormally dilated vessels in the vagina, a bulky
guish UAVM and other types of vascular malformations.44 pulsatile uterus, or pulsating mass in the adnexal area can aid
Moreover, PI3K/AKT and MEK are also vital pathways in an accurate diagnosis.19,53 Injury, biopsy, infection, throm-
leading to cell growth and proliferation in UAVM lesions. bosis, puberty, and pregnancy can cause an acute increase in
Inhibition of these pathways will help reduce UAVM.45–47 severity or flare-ups. Rarely, very high flow damage causes
Most UAVMs are sporadic, which reflects the acuteness of high flow heart failure in early childhood.2,9,51–53
the deficiency, probably resulting in premature embryo
death in the case of transmitting.9,48
Diagnostic Imaging
Imaging modalities to diagnose UAVM such as US, com-
Clinical Presentation puted tomography (CT), magnetic resonance imaging
Vaginal bleeding is the most commonpresentationof UAVM, (MRI), and digital subtraction angiography (DSA) play a
ranging from intermittent spotting to catastrophic hemor- very important role in diagnosis, treatment, and follow-up.
rhage. Menorrhagia, metrorrhagia, menometrorrhagia, and Each imaging modality has its own advantages and disad-
postcoital bleeding have been reported as presenting symp- vantages.Choosing the appropriate technique depends on
toms, which can lead to severe anemia.2,49 Vaginal bleeding the clinical situation and patient comorbidities. In some
in acquired UAVM usually occurs in women who are at cases, using just a single imaging technique is sufficient to
childbearing age, postpartum, or have previous uterine inter- diagnose and evaluate the lesion. However, it is often neces-
ventions.50 A detailed medical history is important to help sary to coordinate many imaging tools to be ensure an accu-
diagnose the UAVM. History of severe uterine bleeding rate diagnosis. The radiological features are summarized in
after curettage in a woman of reproductive age may suggest Table 1.2,19,25,54–62
Hoang et al 5

Figure 3. A 40-year-old female patient was diagnosed with uterine arteriovenous malformation (UAVM) (Yakes type IIA). (A)
Grayscale ultrasound shows subtle myometrial heterogeneity and small anechoic spaces in the myometrium. (B, C) Color Doppler
images manifesting turbulent flow creating a mosaic pattern. (D) Spectral Doppler image shows low-resistance flows.

Grayscale Ultrasound shows the typical features of arteriovenous shunting with

the low-resistance flow. Peak systolic velocity (PSV)
This technique indicates subtle and nonspecific images that ranged from 25 to 110 cm/s with an average of 60.37 cm/s
make it difficult to diagnose a UAVM. The most common and an SD of 26.99 cm/s. Resistive indices ranged from
finding was subtle myometrial heterogeneity, whereas some 0.27 to 0.75 with an average of 0.41 and SD of 0.12
patients might have small anechoic spaces in the myome- (Figures 3 and 4).2,25
trium. Findings of mixed echogenic mass in the uterus are
common and may be mistaken with retained products of
conception(Figures 3 and4).54 Computed Tomography Scans
CT images show that UAVM has the same density as mus-
Color Doppler Ultrasound cle but higher than fat. CT is very useful for those who are
contraindicated with sedatives or MRI. CT is preferred over
Color Doppler reveals a tangle of vessels with the multidi- MRI to evaluate UAVM located near intestinal and skeletal
rectional high-velocity flow making a color mosaic pat- structures. Spiral and multislice CT scans provide fast and
tern. They also show an increased vascularity area in the high-resolution images. High resolution allows for
uterine muscle and a distinct group of vessels coursing the extremely precise measurement, mapping of feeding and
myometrium from the arcuate vessels running perpendicu- draining circuits. However, due to its radioactive nature and
lar to the endometrium. Similar features can also be seen in minimal provision of flow velocity information, its role is
retained products of conception, placental polyp, gesta- limited to emergency cases, or when the MRI is unclear, or
tional trophoblastic disease, and vascular endometrial neo- complementary to the next interventional or surgical plan-
plasm (Figures 3 and 4).55,56 ning (Figures 5 and 6).54,57

Spectral Doppler Ultrasound Magnetic Resonance Imaging

Spectral Doppler images show high peak velocity and low- MRIis a noninvasive and valuable technique that provides
resistance flow. It is often difficult to differentiate the good compatibility with DSA to supportthe diagnosis and
venous and arterial waveform. The study of O’Brien et al25 treatment of UAVM. MRI usually reveals an abnormal
6 Journal of Endovascular Therapy 00(0)

Figure 4. A 35-year-old patient presenting with vaginal bleeding. (A) Grayscale ultrasound reveals multiple cystic structures in the
uterine muscle. (B) Color Doppler image shows a tangle of vessels with the multidirectional high-velocity flow making a color mosaic
pattern. (C, D) Spectral Doppler images show high peak velocity and low-resistance arterial flows (Yakes type IV).

Figure 5. A 61-year-old patient presented with dull lower abdominal pain. (A, B) Axial, (C) coronal maximum intensity projection
(MIP) reconstruction, and (D) 3-dimensional reconstruction contrast-enhanced computed tomography (CT) images in the arterial
phase show contrast agent filling enlarged vessel structures (arrowheads) and aneurysm (arrows) in the right adnexa, myometrium,
and parametrium regions (Yakes type IIIB). The patient has received surgical treatment, which resulted in the postoperative diagnosis
of uterine arteriovenous malformation (UAVM) with an aneurysm. Note that CT scan is preferred in unstable patients with heavy
bleeding, those who cannot afford magnetic resonance imaging (MRI), and when MRI is contraindicated.
Hoang et al 7

Figure 6. Acquired uterine arteriovenous malformation (UAVM) occurred in a 34-year-old patient after an abortion at 20 weeks
due to the fetus was a congenital diaphragmatic hernia. The patient terminated her pregnancy with medication and was experiencing
persistent vaginal bleeding associated with fatigue and dizziness (Yakes type IIA). (A) Non-contrast-enhanced axial computed
tomography (CT) image after 4-month abortion shows a mild heterogeneous hypodensity lesion in the myometrium. (B, C) Axial and
sagittal contrast-enhanced CT images at the arterial phase show strong enhancing lesion with zigzag blood vessels (arrows).

tangle of blood vessels with early contrast enhancement. detail from any desired direction and fully display the pro-
Advanced techniques with high-resolution bright-blood and cess of filling and draining at intervals. 4D-DSA can expand
black-blood sequential magnetic resonance angiography the possibilities of bleeding risk assessment and help plan
(MRA) (with or without contrast agent) have allowed a treatment through an improved understanding of vascular
clear view of the feeding arteries and draining veins and anatomy. Furthermore, this technique can reduce the dose
nidus. MRA with 3-dimensional (3D) and dynamic pulse of radiation and contrast agent needed for angiographic
sequences with multiplane reconstruction and timing reso- evaluation (Figures 12–14).61,62
lution play an important role in the evaluation of UAVMs
(Figures 7–11).19,58–60
Management
Once the accurate diagnosis of a UAVM is given, the
Digital Subtraction Angiography management principle depends on the hemodynamic sta-
This method is not only the gold standard in diagnosing tus, degree of bleeding, patient age, and desire for future
UAVM but also an interventional treatment technique.33,61 fertility.63,64 In the case of unstable hemodynamics, intrave-
There have been several studies in the literature regarding nous fluid resuscitation must be initiated as well as blood
creating 4D-DSA images from 3D-DSA images obtained products must be used early in the process.65 A Foley cath-
with time resolution. This technique gives the reader a bet- eter can work to stem the bleeding in the situation of life-
ter ability to identify characteristicsof the lesion than a 3D threatening hemorrhage.66 Patients with minor bleeding and
technique. With 4D-DSA, the planning stage of interven- stable hemodynamic status can receive conservative treat-
tion can be simplified. Viewers can analyze the nidus in ment. Many of these patients will have no symptoms,
8 Journal of Endovascular Therapy 00(0)

Figure 7. A case of acquired uterine arteriovenous malformation (UAVM) lesion associated with placental retention after miscarriage
(Yakes type IIA). (A) Coronal T2 turbo spin echo (TSE) image shows a heterogeneous hyperintensity lesion approximately 19×25 mm
in size (red arrow). (B) Contrast-enhanced sagittal T1 TSE Fat Sat image shows the strong heterogeneous enhancement in the lesion
(red arrow). (C, D) Postcontrast maximum intensity projection (MIP) reconstruction images show that the lesion has early venous
drainage (blue arrowhead), a typical feature of the UAVM (red arrows).

suggesting that the microlesion UAVM resolves on its One case report describes treatment response to a gonadotro-
own.30 Angiography and embolization should be considered phin-releasing hormone agonist following an unsuccessful
in patients presenting anemic, recurrent bleeding, or hemo- course of methylergonovine maleate.2,67,70
dynamically unstable.32 The scheme of diagnostic and treat-
ment are shown in Figure15.19,21,44–48,63–70
Endovascular Treatment
Uterine artery embolization can be performed in patients
Conservative Treatment who are hemodynamically unstable and require blood trans-
The use of methylergonovine maleate for 1 year has been fusion.21,61 Embolization is preferred over open surgery as
successful in treating UAVM.67 Besides, there are many the initial approach due to it being minimally invasive and
studies on the use of different drugs and hormone therapies fertility preserving. Transcatheter arterial embolization has
that are effective in the treatment of UAVM.9 It is thought been shown in multiple studies to be highly successful in
that danazol therapy reduces blood flow to artery malforma- treating both vaginal and lower intestinal bleeding caused
tions, allowing for thrombogenic injury.68 Combined oral by UAVM.71–73
contraceptive pills have been used successfully in these The most commonly used embolic agent was polyvinyl
cases showing reversal of lesions 3 months after treatment.69 alcohol particles. Other embolic agents included coils or
Hoang et al 9

Figure 8. A 38-year-old patient having uterine arteriovenous malformation (UAVM) with pseudoaneurysm complications had been
treated with digital subtraction angiography (DSA) and surgery (Yakes type IIIB). (A) Coronal T2 turbo spin echo (TSE), (B) axial T2
TSE Fat Sat, and (C) sagittal T1 TSE Fat Sat images show that the lesion has a heterogeneous intensity signal with zigzag blood vessels.
Adjacent, the lesion has a pseudoaneurysm of 21.3 mm in diameter (arrows). Postcontrast (D) axial, (E) coronal maximum intensity
projection (MIP), and (F) 3-dimensional reconstruction images reveal UAVM (arrows) and pseudoaneurysm (circles) more clearly.

Figure 9. Uterine arteriovenous malformation (UAVM) was diagnosed in a young patient born prematurely at 27 weeks gestation
(Yakes type IV). (A, B) Sagittal and axial T2 turbo spin echo (TSE) images show multiple meandering vessels in the myometrium and
parametrium. These vessels have a high flow velocity manifested with a flow-void effect (red arrows). (C) Coronal T2 TSE Fat Sat

Figure 9. (continued)
10 Journal of Endovascular Therapy 00(0)

Figure 9. (continued)
image shows that proliferative vessels with high flow in lesion have hypointensity signal (red arrows), the arch and cycle veins have a
high signal (blue arrows), and thickness of myometrium in the left corner of the uterus corresponding to the lesion is very thin (yellow
arrow). (D) Axial T1 TSE Fat Sat image shows the lesion with heterogeneous hypointensity and flow-void. (E, F) Contrast-enhanced
T1 TSE Fat Sat images show vivid heterogeneous enhancement of UAVM in the uterus and parauterus (red and blue arrows). (G, H)
Contrast-enhanced dynamic magntic resonance angiography (MRA) images with coronal maximum intensity projection (MIP) show
that the nidus of UAMV is fed by uterine arteries (red arrows), numerous vessels proliferate inside and around the lesion, and there is
not early drainage via the system veins (ovarian and pelvic veins) in this phase. The patient had received surgical treatment.

Figure 10. A patient had acquired uterine arteriovenous malformation (UAVM) after a gestational abortion at 7 weeks of gestation
(Yakes type IIA). Human chorionic gonadotrophin (HCG) test was negative and she had no vaginal bleeding. (A, B) Sagittal and
coronal magnetic resonance imaging (MRI) T2 turbo spin echo (TSE) images show thickened myometrial layers and flow-void signal
uneven appearance. (C, D) Sagittal and coronal contrast-enhanced T1 TSE Fat Sat images show a heterogeneous enhancement of the
lesion. (E) Contrast-enhanced dynamic magnetic resonance angiography (MRA) images with TWIST (time-resolved angiography with
interleaved stochastic trajectories) technique show that UAMV is fed by arteries (red arrow) and is early drained by enlarged veins
(blue arrow). The ovarian vein appeared at 34.9 seconds after contrast administration (blue arrow).

micro coils, Glue/N-butyl cyanoacrylate, gel foam or gela- preserved for women who show failure in embolization ther-
tines sponge, histoacryl and lipiodol and alcohol.9,74 In gen- apy and have no desire to conserve their fertility.9,21 Open
eral, the treatment of UAVM embolism should be based on hysterectomy is considered an invasive procedure. With the
the Yakes classification system (Table 2).7,75,76 Current tech- emergence oflaparoscopic approach, hospital stay, patient
niques for intravascular diagnosis and treatment often use morbidity and mortality associated with hysterectomy have
DSA to pass microcatheters from the femoral artery up to reduced significantly.19,74,79 Methods of isolating and bipolar
UAVM lesions and then inject contrast material for diagno- coagulation of uterine vessels within US monitoring show a
sis. Bio-glue is then used to embolize the UAVM. In cases significantly minimized lesion and decreased blood flow.2,27
of high-flow UAVMs or uterine arteriovenous fistulas, coils Selective embolization before surgery can provide good
may be used in combination with other embolism agents.9,77 control of UAVM (Figure 11).80,81
Another effective endovascular approach is balloon-
occluded retrograde transvenous obliteration (BRTO).
Genes Therapy
UAVM-reduction therapy is performed entirely through
BRTO by injection of a sclerosant (Figures 12–14).78 The recently identified molecular pathway involved in the
development of these potential lesions inhibition factors
may improve the treatment problem.82,83 One proposed
Surgical Treatment hypothesis is that endothelial dysfunction that produces
Although hysterectomy is thedefinitivetreatment for UAVM, AVM is caused by increased activity of the kinase MAP2K1,
it is no longer considered the first-line treatment and generally also known as MEK1. MEK1 inhibitors are used in cancer
Hoang et al 11

Figure 11. A 29-year-old patient was diagnosed with uterine arteriovenous malformation (UAVM), whose human chorionic
gonadotrophin (HCG) ranged between 110 to 120 mIU/mL through 4 tests in 10 days (Yakes type IV). (A) Sagittal T2 turbo spin echo
(TSE), (B) axial T2 TSE Fat Sat, (C) sagittal T1-Vibe Fat Sat images show an abnormal vascular cluster in the right mesovarium with the
right oviduct dilated at 1.6 cm diameter (circles). The lesion like soft tissue structures filled with low signal on T1-weighted (T1W)
images, high signal on T2W images. The right ovary shows a hemorrhagic follicle 23×26 mm in size (red asterisks). Postcontrast (D)
sagittal and (E, F) axial T1 TSE Fat Sat images show strong heterogeneous enhancement of lesion (blue arrows). (G, H) The patient
underwent surgery for the lesion removal and hemorrhagic cystic ovarian dissection. Surgery and histology confirmed the diagnosis of
UAVM acquired from an ectopic pregnancy.

Figure 12. A patient had menorrhagia after a 15-week-fetus abortion by misoprostol due to fetal anomalies. After 2 months,
human chorionic gonadotrophin (HCG) test was 22 mIU/mL and hemoglobin level in the blood was 95 g/L. Ultrasound showed a
mixed echogenic structure and hypervascularity in the uterine (not shown). (A) Sagittal and (B) coronal T2 turbo spin echo (TSE)
images show heterogeneous hypointensity signal lesions. Contrast-enhanced (C) axial, (D) sagittal, (E) coronal, and (F) 3-dimensional
reconstruction T1 TSE Fat Sat images show a vascular-rich lesion that is a zigzag and vivid enhancement. (G, H) The patient received
successful digital subtraction angiography (DSA) intervention (Yakes type IIA).
12 Journal of Endovascular Therapy 00(0)

Figure 13. Patients presented with menorrhagia after an abortion at 6 weeks gestation. The diagnosis based on human chorionic
gonadotrophin (HCG) test (111 mIU/mL) and ultrasound (US) findings was placental retention and she was treated with the medical
method. Three weeks after the abortion, HCG was 43 mIU/mL. US images showed that the uterine fundus had mixed anechoic
plates and increased blood vessel signals (not shown). She continued to receive medical treatment. Seven weeks after the abortion,
HCG was 8 mIU/mL and she had a magnetic resonance imaging (MRI) scan. (A–D) Contrast-enhanced MRI and magnetic resonance
angiography (MRA) images showed that the lesion is typical uterine arteriovenous malformation (UAVM). DSA was then conducted
for diagnosis and treatment. (E–G) Preembolization DSA images showed UAVM lesions in the form of zigzag tufts of blood vessels. (F)
Postembolization DSA image showed that the lesion had disappeared (Yakes type IV).

Figure 14. A 42-year-old patient had a hemorrhage after the induced abortion at more than 15 weeks of fetus with defects. She had
got emergency bilateral artery suture hemostasis of the uterus. A month later, she presented with abnormal vaginal bleeding (Yakes
type IIA). (A) Grayscale ultrasound shows myometrial mixed echogenicity, multiple dilated tubular structures spreading throughout
myometrium. (B) Color Doppler image shows many areas of increased vascularity, aliasing dilated vessels; arterial and venous
spectral waves are indistinguishable. (C) Coronal magnetic resonance imaging (MRI) T2 turbo spin echo (TSE) image shows multiple
Figure14. (continued)
Hoang et al 13

Figure14. (continued)
meandering vessels in the myometrium and parametrium. The uterine wall is also slightly thick. (D) Axial MRI short tau inversion
recovery (STIR) image shows that venous flows have a high signal intensity and arterial high flows have no signal due to flow-void
effect. (E) Preembolism DSA shows an abnormal blood vessel tangle with early contrast enhancement, a typical feature of uterine
arteriovanous malformation (UAVM). The lesion is embolized by coils, glue, and gel foam via the microcatheters. (F) Postembolization
DSA shows the size of the blood tangle declined and no early draining vein. (G, H) Contrast-enhanced axial and 3-dimensional
computed tomography (CT) images after 6 months of treatment show that the UAVM lesion is completely resolved. The coils in the
blood vessel are also observed (circles).

Figure 15. Approach to diagnosis and treatment of uterine arteriovenous malformation (UAVM).19,21,44–48,63–70
14 Journal of Endovascular Therapy 00(0)

Table 2. The Arteriovenous Malformation (AVM) Embolism Strategy Is Based on the Yakes Classification System.7,75,76

Type Treatment Approach

I Aretriovenous fistula can be permanently embolized by mechanical occluding devices such as umbrellas, coils. Ethanol can
be used independently if the diameter is small.
IIA Transcatheter ethanol embolization.
IIB Transcatheter ethanol embolization and coiling aneurysmal outflow vein.
IIIA Coiling single aneurysmal outflow vein; ethanol can be used.
IIIB Coiling each outflow vein; reverse intravenous catheterization can be used.
IV Transcatheter super-selective embolization with ethanol.

can self-monitor for bleeding status, menstrual cycle, and

follow-up for any other unusual symptoms.25
According to the review by Rebeka Eling et al,9 28
patients included in the study had a total of 35 pregnancies;
among these 32 infants were born to mothers post UAVM
diagnosis. Five of these pregnancies (13.9%) ended in mis-
carriage. Five (13.9%) had postnatal complications. Eight
(22.9%) had antenatal complications, including difficulties
conceiving and premature labor. Ten pregnancies (28.5%)
reported no complications either antenatally or postnatally.
Figure 16. Interfering in the pathways of uterine arteriovenous A total of This study is an important step in looking at how
malformation (UAVM) formation and development by using to maximize fertility following UAVM treatment. However,
inhibitory factors can treat the UAVM lesion.37–48 several other factors, such as maternal age and other causes
of infertility, will incorrectly affect the pregnancy rate fol-
and may have potential applications in AVM. In addition, lowing diagnosis and treatment of UAVM.
inhibition of the PI3K/AKT and Ras/MAP kinase pathways US is a cost-effective imaging method for surveillance.
may also be effective gene therapy but is under study CT and MRI are also needed for detailed evaluation. If
(Figure 16).37–48 symptoms persist and the disease recurs, reembolizationor
radical surgery should be considered.87–91

Complications Conclusion
Treating UAVM with embolization has fewer complications UAVM is a rare cause of uterine bleeding in reproductive
than surgical management. Reported complications include age women which can lead to a life-threatening condition.
uterine infection, uterine ischemia, uterine necrosis, damage US is an effective tool for screening and initial assessment
to other organs, and possible problems in future pregnancies when UAVM is suspected. The characteristics of UAVMs
(eg, abnormalities of the placenta).1,9 Hysterectomy, the most are increased vascular and dilated blood vessels throughout
common gynecologic procedure, also has its own complica- uterine muscles. Pelvic DSA is the present gold standard for
tion, including infectious, venous thromboembolic, genito- the diagnosis of UAVM, which also helps determine the
urinary and gastrointestinal tract injury, recurrent bleeding, main feeding vessels in case of the consideration of emboli-
and nerve injury.84 Another concern is ovarian failure condi- zation treatment. Conservative treatment, endovascular
tion after the uterine arterial constriction. However, this can intervention, and surgery are choices for management up to
be avoided by isolating and ligating uterine arteries selec- the individual situation.
tively, excluding the possibility of blocking the utero-ovarian
communicating artery.19,85 Several studies have concluded Author Contributions
that pregnancy is possible after uterine artery constric- The authors contributed equally.
tion.9,18,19 Uterine curettage should be eliminated due to its
persistent hemorrhage caused by the disruption of the thin Declaration of Conflicting Interests
layer of endometrium covering the malformation.21,86 The author(s) declared no potential conflicts of interest with respect
to the research, authorship, and/or publication of this article.
Follow-up Funding
The follow-up period is variable depending on patient con- The author(s) received no financial support for the research,
dition, typeof treatment, fertility check, and so on.17 Patients authorship, and/or publication of this article.
Hoang et al 15

ORCID iD 15. Hilal K, Masroor I, Aziz A, et al. Acquired vascular mal-

formation in ruptured caesarean section scar: a rare cause
Van Trung Hoang https://orcid.org/0000-0001-7857-4387
of life-threatening vaginal bleeding. BMJ Case Rep.
2013;2013:bcr2013009489. doi:10.1136/bcr-2013-009489
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