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K E Y W O R D S: 3D US; congenital uterine malformations; magnetic resonance; MRI; Mullerian; Müllerian anomalies;
Müllerian duct anomalies; three-dimensional ultrasonography; UM; uterine malformations
Results Using 3D ultrasound we diagnosed: one case Uterine malformations make up a heterogeneous group
with uterine agenesis; 10 with unicornuate uterus, four of of congenital anomalies that can result from the
which also underwent MRI; six with didelphic uterus, one underdevelopment of the Müllerian ducts, disorders in
of which had MRI; 45 with bicornuate uterus, 12 of which their fusion and/or alterations in septum resorption.
had MRI; 125 with septate uterus (18 with two cervices), The prevalence of uterine malformations is difficult
42 of which had MRI (six with two cervices); 96 with to establish. They are estimated to occur in 0.4%
arcuate uterus, three of which had MRI; and three with (0.1–3%)1,2 of the general population and in 4%
diethylstilbestrol (DES) iatrogenic uterine malformations, of infertile women (some authors do not distinguish
all of which had MRI. Among the 65 which underwent between these two groups3 ), and in patients with
MRI, the diagnosis was: four cases with unicornuate repeated spontaneous miscarriages the figures fluctuate
uterus, 10 with bicornuate uterus (two with two cervices), between 3 and 38%4 – 8 . The discrepancy among different
45 with septate uterus (five with two cervices), three publications stems from their use of different diagnostic
with arcuate uterus and three with DES-related uterine techniques, heterogeneous population samples and the
malformations. The concordance between 3D ultrasound clinical diversity of Müllerian anomalies.
and MRI was very good (kappa index, 0.880 (95% There are several classifications of uterine malforma-
CI, 0.769–0.993)). Discrepancies in diagnosis between tion, but the most widely accepted is that established in
Correspondence to: Dr C. Bermejo, Gabinete Médico Velázquez, Velazquez 25, 1◦ , 28001 Madrid, Spain
(e-mail: carminabermejo@yahoo.es)
Accepted: 28 August 2009
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
594 Bermejo et al.
1988 by the American Fertility Society (AFS)9 , which is Médico Velázquez, Madrid, Spain and Delta Ecografı́a
not only based on embryological factors, but also takes Madrid, Spain). They had been referred to our clinics
into account clinical factors, prognosis and treatment on suspicion of uterine malformation following clini-
(Figure 1). It classifies uterine malformations into seven cal and/or conventional two-dimensional (2D) ultrasound
groups, providing a very useful, but somewhat incom- examination. We performed 3D ultrasound in all cases,
plete, categorization, as it requires the specification of any bimanual examination and speculoscopy in 283 cases and
associated malformations, when found. MRI in 65.
There are several techniques available for the evaluation
of uterine malformations. When the cavity only is to be
3D ultrasound examination of uterine cavity
assessed, hysterosalpingography (HSG) and hysteroscopy
and cervical canal
are especially useful. Laparotomy and laparoscopy can be
also used for examination of the uterine fundus. There are Examinations were performed using a Voluson Pro and
two techniques, however, that combine the study of both three Voluson 730 Expert (GE Medical Systems, Zipf,
these structures, which is indeed relevant for the diagnosis: Austria) ultrasound machines, equipped with convex
magnetic resonance imaging (MRI) and three-dimensional transabdominal probe RAB4-8L 4–8 MHz 4D and
(3D) ultrasound. While MRI is a useful option in the endocavitary probe RIC5-9H 5–9 MHz 4D. In all cases
diagnosis of Müllerian anomalies, with numerous studies (except for three patients with intact hymen), we obtained
having proved its excellent efficacy in this field10 – 13 , transvaginally between one and three static volumes of the
3D ultrasound represents a valid alternative, because, uterus, with a quality ranging from medium to maximum.
in addition to its lower cost and better tolerance by Initially we visualized the uterus on 2D ultrasound in
patients, it provides images of very similar quality to those a strict mid-sagittal view, adjusting the capture window
yielded by MRI14 . There is a lack, however, of studies to obtain the optimal 3D volume. The volume was then
comparing these two techniques for the diagnosis and obtained using a sweep angle of 90◦ from one side of the
categorization of uterine malformations. The objective of uterus to the other, bisecting the capture plane (Figure 2).
this study, therefore, was to demonstrate the value of 3D In 25 cases with anomalies resulting in a large transverse
ultrasound in the diagnosis of uterine malformations and uterine diameter (didelphic uterus (n = 5), wide septate
its concordance with MRI. uterus (n = 10), bicornuate uterus with ample separation
between horns (n = 8) and communicating unicornuate
METHODS uterus (n = 2)) the volume was obtained from a transverse
plane so that both uterine horns could be visualized,
Included in this study were 286 women diagnosed with in order to allow better estimation of the cavity/fundus
uterine malformation by 3D ultrasound between Novem- relationship in the 3D reconstruction (Figure 3). In seven
ber 2004 and May 2009 in one of two centers (Gabinete cases (with optimal ultrasound conditions including low
Figure 1 Classification of uterine malformations according to the American Fertility Society9 . DES, diethylstilbestrol.
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
3D ultrasound and MRI in uterine anomalies 595
Figure 2 Procedure to obtain a rendered image of a Müllerian anomaly, in this case an arcuate uterus. (a) The initial plane for obtaining
three-dimensional volumes was generally mid-sagittal (Window A). Acquisition was carried out with a sweep angle of 90◦ . The image
corresponds to the bisector of the angle made by the volumetric probe as it is moved from one side of the uterus to the other. Window B is
the axial plane and Window C the coronal plane. (b) The rendering box was then adjusted (Window A) and the green line adapted to the
curved plane of the uterine cavity so it became positioned on the endometrium. The midline was verified (Window B). In the bottom right is
the rendered image of the surface of the arcuate uterus.
Figure 3 In uterine malformations with a large transverse diameter, such as this bicornuate uterus, three-dimensional (3D) volumes were
generally obtained from an axial plane (Window A) so that both horns would fit in the same field of view, enabling the cavity/fundus
relationship to be better established in the 3D reconstruction (bottom right).
body mass index) and in the three patients with intact When studying the cervix we readjusted the rendering
hymen, we captured the volume transabdominally, with box and the green line. When the volume was obtained
initial sagittal, coronal or transverse planes, and in 25 in a transverse plane, we included both uterine horns in
cases we obtained two volumes, one to study the fundus the rendering box and adjusted the green line so that a
and cavity and another to study the cervix and cervical good quality image showing both cavity and fundus was
canal (Figure 4). The volumes were manipulated until obtained in the rendered view. Luminosity and contrast
a satisfactory surface rendered image was obtained of curves were adjusted for both multiplanar and rendered
the fundus and uterine cavity as well as the cervical images, as well as for threshold and transparency. The
canal. When a mid-sagittal plane was used to capture rendering modes used were a mixture of surface/gradient
the volume, we adjusted the rendering box in Window of light of 10/60 to 60/10.
A (capture image) to include the uterine fundus and
adjusted the green rendering line (from front to back), Physical examination
tracing the sagittal curve plane of the uterine cavity so that
the line was located on the endometrium, and checking With the exception of the three patients with intact
in Window B that we were in the midline (Figure 2). hymen, patients underwent bimanual examination and
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
596 Bermejo et al.
Figure 4 Three-dimensional surface rendered ultrasound images of the uterine cervix in three women with uterine malformations:
(a) incomplete cervical septum in a case of septate uterus; (b) complete cervical septum in a case of septate uterus; (c) two diverging cervical
canals in a case of septate uterus with two cervices.
speculoscopy before and/or after the ultrasound exami- Findings were classified according to the AFS9
nation to confirm the ultrasound findings. We looked for (Figures 1 and 5), describing the associated malformations
associated findings, i.e. vaginal septum, cervical septum found. In order to distinguish bicornuate from septate
or duplicity and abnormal pelvic masses. uteri using 3D ultrasound we used the formula proposed
by Troiano and McCarthy15 : a line was traced, joining
Magnetic resonance imaging both horns (Figure 6). If this line crossed the fundus
or was ≤ 5 mm from it, the uterus was considered
Sixty-five patients underwent MRI after 3D ultrasound bicornuate, while if it was > 5 mm from the fundus, the
and physical examinations. MRI was indicated for uterus was considered septate, regardless of whether the
patients with previous poor obstetric outcome (two fundus was dome-shaped, smooth or discretely notched
or more spontaneous miscarriages, premature birth or (Figure 6). When differentiating bicornuate from septate
impossibility to accomplish pregnancy) and for those uteri using MRI, all cases with an incision > 1 cm
with complex anomalies (Table 1). The examination was
deep in the fundus were considered to be bicornuate
performed by the same observer (E.L.) in all cases, using
uterus. Differentiation between arcuate and septate uteri
a Siemens Magneton Avanto 1.5 Tesla machine (Siemens
was carried out in the coronal plane on both 3D
Medical Solutions, Mountain View, CA, USA). All studies
included coronal high-resolution T2-weighted turbo spin- ultrasound and MRI. While both types of uterus have a
echo imaging with the following parameters: TR/effective normal contour, in arcuate uterus the fundal indentation
TE, 3410/114; refocusing flip angle, 180◦ ; turbo factor, appears as an obtuse angle at the central point16 , with
25; rectangular field of view, 250 × 100 mm; matrix, a depth of up to 1.5 cm17 , whereas septate uterus is
320 × 320; slice thickness, 4 mm; 195 Hz/pixel; 19 slices; characterized by a fundal indentation with an acute angle
1–3 signal averages; average time of acquisition, 2 min at the central point, with a depth of 1.5 cm or more
49 s. (Figure 7).
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
3D ultrasound and MRI in uterine anomalies 597
Figure 5 Three-dimensional surface rendered ultrasound images showing different types of uterine malformation using the American
Fertility Society9 classification: (a) normal uterus; (b) unicornuate uterus (Type IId); (c) didelphic uterus (Type III); (d) complete bicornuate
uterus (Type IVa); (e) partial bicornuate uterus (Type IVb); (f) septate uterus with two cervices (Type Va); (g) partial septate/subseptate
uterus (Type Vb); (h) arcuate uterus (Type VI); and (i) uterus with diethylstilbestrol (DES) drug-related malformations (Type VII).
Table 2 Diagnosis of uterine malformations on three-dimensional (3D) ultrasound and magnetic resonance imaging (MRI)
Agenesis 1 0 —
Unicornuate uterus 10 (2 communicating) 4 (1 communicating) 4 (1 communicating)
Didelphic uterus 6 1* 0
Bicornuate uterus 45 (1 with two cervices) 12† 10 (2 with 2 cervices)
Septate uterus 125 (18 with 2 cervices) 42 (6 with 2 cervices) 45 (5 with 2 cervices)
Arcuate uterus 96 3 3
Iatrogenic uterine malformations 3 3 3
Total 286 65 65
*One of the three patients who were not examined clinically was diagnosed as having didelphic uterus on 3D ultrasound but was found to
have bicornuate uterus with two cervices on MRI. †Three uteri diagnosed as bicornuate on 3D ultrasound were found to be septate on MRI.
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
598 Bermejo et al.
Figure 6 To distinguish bicornuate uteri from septate uteri with three-dimensional ultrasound we used the formula proposed by Troiano and
McCarthy15 : a line was traced joining both horns of the uterine cavity. If this line crossed the fundus or was ≤ 5 mm from it, the uterus was
considered bicornuate (a and b); if it was > 5 mm from the fundus it was considered septate, regardless of whether the fundus was
dome-shaped (c), smooth or discretely notched.
DISCUSSION
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
3D ultrasound and MRI in uterine anomalies 599
Figure 8 Comparison of three-dimensional ultrasound and magnetic resonance imaging in cases of uterine malformation; the two imaging
modalities are extremely similar. Images, according to the American Fertility Society9 classification, show: (a) unicornuate uterus (Type IId);
(b) bicornuate bicollis uterus (Type IVb); (c) septate uterus with two cervices (Type Va); (d) partial septate uterus (Type Vb); (e) uterus with
diethylstilbestrol (DES) drug-related malformations (Type VII).
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
600 Bermejo et al.
Figure 10 Septate uterus with two cervices on three-dimensional surface-rendered ultrasound (a and d) and magnetic resonance imaging (b,
c, e and f). Axial plane showing the two cervices can be observed in (e) and sagittal planes of the two hemiuteri, each with a cervix, can be
observed in (c) and (f).
accuracy/efficacy, giving 3D ultrasound the advantage whether some intermediate forms should be assigned to
over MRI as it is cheaper and better tolerated by patients. Group V or Group VI, as some deeply arcuate uteri could
Furthermore, the gynecological examination is simple and be partially septate with a short, thick septum. Markedly
is part of our usual work-up. arcuate uteri have a worse reproductive prognosis than
3D ultrasound was of most use when distinguishing do those with a minor cavitary incision, as Troiano and
between arcuate, septate and bicornuate uteri. Alcázar28 McCarthy15 and Salim et al.29 found.
confirmed this, also noting its lower accuracy in diagnos- Our study was limited by the fact that the radiologist
ing didelphic uteri. However, the differential diagnosis who carried out the MRI examination was not blinded to
between these three it is not always easy for 3D ultrasound the 3D ultrasound diagnosis, and only those cases found
or MRI. There are intermediate and incomplete forms of to be positive for uterine malformations by 3D ultrasound
bicornuate and septate uteri, due to simultaneous lack of were later analyzed by MRI. Thus, we remain ignorant
fusion and reabsorption of Müllerian ducts. For example, as to whether any of the negative cases on 3D ultrasound
septate uteri with very wide septa have a large separation would have proved positive on MRI.
between the horns, and the structure of the septum on We believe that 3D ultrasound is a useful complement
ultrasound is similar to that of myometrium. In these to 2D ultrasound on many occasions in gynecology, but
cases, the morphology of the cavity and the type of signal that it is in the diagnosis of uterine malformations that it is
obtained from the septum on MRI, indicating the pres- fundamental. We propose that, on suspicion of Müllerian
ence of myometrium, which is theoretically only present anomalies, 3D ultrasound be carried out, accompanied by
in the wall of bicornuate uteri, would lead to an incor- complete gynecological examination. In doubtful or com-
rect diagnosis of bicornuate uterus. Applying Troiano and plex cases, MRI should be performed, particularly for the
McCarthy’s15 formula to distinguish between these two assessment of the cervix and vagina. Surgery should be
types would allow the correct diagnosis of septate uterus reserved for malformations that could benefit from this
to be made (Figure 11). We found it difficult to decide treatment.
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.
3D ultrasound and MRI in uterine anomalies 601
Copyright 2010 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2010; 35: 593–601.