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TECHNIQUES AND INSTRUMENTATION

Accuracy of three-dimensional ultrasound in diagnosis


and classification of congenital uterine anomalies
Tullio Ghi, M.D., Ph.D., Paolo Casadio, M.D., Marina Kuleva, M.D., Anna Myriam Perrone, M.D.,
Luca Savelli, M.D., Susanna Giunchi, M.D., Maria Cristina Meriggiola, M.D.,
Giampietro Gubbini, M.D., Gianluigi Pilu, Professor, Carla Pelusi, Professor, and
Giuseppe Pelusi, Professor
Department of Obstetrics and Gynecology, University Hospital of Bologna, Italy

Objective: To assess the accuracy of three-dimensional (3D) ultrasound in the diagnosis of congenital uterine
anomalies.
Design: Prospective study.
Setting: University hospital.
Patient(s): Nulliparae with three or more consecutive miscarriages.
Intervention(s): All women underwent 3D transvaginal ultrasound study of the uterine cavity.
Main Outcome Measure(s): Women with negative ultrasound findings subsequently underwent office hysteroscopy,
whereas a combined laparoscopic-hysteroscopic assessment was performed in cases of suspected M€ ullerian anomaly.
Result(s): A specific M€ullerian malformation was sonographically diagnosed in 54 women of the 284 included in
the study group. All negative ultrasound findings were confirmed at office hysteroscopy. Among the women with
abnormal ultrasound findings, the presence of a M€ ullerian anomaly was endoscopically confirmed in all. Concor-
dance between ultrasound and endoscopy around the type of anomaly was verified in 52 cases, including all those
with septate uterus and two out of three with bicornuate uterus.
Conclusion(s): Volume transvaginal ultrasound appears to be extremely accurate for the diagnosis and classifica-
tion of congenital uterine anomalies and may conveniently become the only mandatory step in the assessment of
the uterine cavity in patients with a history of recurrent miscarriage. (Fertil Steril 2009;92:808–13. 2009 by
American Society for Reproductive Medicine.)
Key Words: Three-dimensional ultrasound, congenital uterine anomalies, recurrent miscarriage, office hystero-
scopy and laparoscopy

M€ullerian anomalies include a wide group of congenital ally been the most widely used method in the differential
uterine malformations whose prevalence in the general pop- diagnosis of M€ullerian malformations (8).
ulation is around 3%–4% (1, 2). Most of them are reported to
Recently, thanks to the introduction of volume ultrasound,
increase the risk of infertility or adverse pregnancy outcome
a comprehensive evaluation of uterine morphology has be-
(2–6). The reproductive outcome and treatment options
come feasible at transvaginal ultrasound (9). At volume ultra-
depend on the type of uterine malformation.
sound, both the external contours and internal morphology of
As the most common classification of M€ ullerian anomalies the uterus may be displayed on the coronal plane, and the
is in accordance with either the external or internal morphol- presence and type of uterine anomaly may be accurately
ogy of the uterus (7), assessment of both is mandatory for detected. The purpose of this study was to evaluate in a se-
a correct diagnosis of the type of malformation. Despite lected group of women the accuracy of volume ultrasound
being invasive, a combined hysteroscopic and laparoscopic in the diagnosis and classification of M€ullerian anomalies.
evaluation of uterine morphology and contour has tradition-

Received January 16, 2008; revised May 22, 2008; accepted May 27, MATERIALS AND METHODS
2008; published online August 11, 2008.
From January 2004 to December 2006, all women consecu-
T.G. has nothing to disclose. P.C. has nothing to disclose. M.K. has noth-
ing to disclose. A.M.P. has nothing to disclose. L.S. has nothing to dis- tively referred to our infertility clinic who were nulliparae
close. S.G. has nothing to disclose. M.C.M. has nothing to disclose. with a history of recurrent miscarriage (three or more consec-
G.G. has nothing to disclose. G.P. has nothing to disclose. C.P. has utive abortions by 12 weeks of gestation) were prospectively
nothing to disclose. G.P. has nothing to disclose.
Reprint requests: Tullio Ghi, M.D., I Clinica Ostetrica-Ginecologica, Policli-
enrolled in the study and submitted to a volume ultrasound
nico S.Orsola-Malpighi, Via Massarenti, 13, 40100 Bologna (FAX: evaluation of the uterine cavity in the midluteal phase of
39-051-636-4411; E-mail: tullioghi@yahoo.com). the cycle. Patients were excluded if uterine fibroids or

808 Fertility and Sterility Vol. 92, No. 2, August 2009 0015-0282/09/$36.00
Copyright ª2009 American Society for Reproductive Medicine, Published by Elsevier Inc. doi:10.1016/j.fertnstert.2008.05.086
endometrial polyps were incidentally detected at ultrasound. to maximum quality. Each volume data set was stored on
For each patient, a control of uterine cavity by office hystero- the hard disk of the ultrasound machine and made available
scopy was arranged in the early follicular phase of the subse- for offline analysis by one of authors (TG or MK).
quent cycle.
As shown in Figure 1, the volume reconstruction technique
Hysteroscopy and ultrasound were performed by different was standardized according to the following criteria: the vol-
operators (hysteroscopy by PC, ultrasound by TG) with se- ume rendering box as narrow as possible in the sagittal plane
lective competence for each technique. Ultrasound findings and adjusted on the uterine corpus in the coronal plane, cut
were not made available to the operator doing the hystero- plane scrolled in anterior-posterior fashion with slice thick-
scopy. Whenever a specific uterine malformation was sono- ness set at 1 cm, transparency low (<50%), and volume ren-
graphically diagnosed, a combined laparoscopic- dering by a mix of surface and maximum mode. The analysis
hysteroscopic evaluation instead of office hysteroscopy was of uterine morphology was performed in a standardized re-
proposed to the patient and arranged within a month from ul- formatted section with the uterus in the coronal view using
trasound. The study was approved by the Institutional Review the interstitial portions of fallopian tubes as reference points.
Board of our hospital. In addition, a signed declaration of no Specific ultrasound diagnosis of uterine anomalies was based
conflict of interest has been provided by all the authors in- on the classification system originally proposed by the Amer-
volved in the study. ican Fertility Society and subsequently modified according to
3D ultrasound landmarks (10) (Table 1).
Ultrasound scan was performed using a Voluson 730 Ex-
pert and a Voluson 730 Pro machine (GE, Milan, Italy) equip-
ped with a multifrequency volume endovaginal probe. The RESULTS
insonation technique was standardized according to the fol- During the study period, 312 nulliparae attending our center
lowing criteria: probe frequency set at 9 mHz, a midsagittal with a history of recurrent abortions were submitted to trans-
view of the uterus filling 75% of the screen, three-dimen- vaginal volume ultrasound. In 28 cases, women were consid-
sional (3D) box size including the uterus from fundus to ered not eligible for the study owing to incidental detection of
the cervix, sweep angle of 90 , and sweep velocity adjusted uterine fibroids (n ¼ 19) or endometrial polyps (n ¼ 9) at

FIGURE 1
Multiplanar imaging of a normal uterus at volume ultrasound: the volume rendering box is as narrow as possible in
the sagittal plane (panel B) and adjusted on the uterine corpus in the coronal plane (panel A). A rendered image of
the normal uterus on the coronal plane is displayed on panel D.

Ghi. 3D ultrasound in M€
ullerian anomalies. Fertil Steril 2009.

Fertility and Sterility 809


TABLE 1
Classification of congenital uterine anomalies according to volume transvaginal ultrasound (10).
Uterine morphology Fundal contour External contour
Normal Straight or convex Uniformly convex or with indentation
<10 mm
Arcuate Concave fundal indentation with Uniformly convex or with indentation
central point of indentation at <10 mm
obtuse angle (>90 )
Subseptate Presence of septum, which does not Uniformly convex or with indentation
extend to cervix, with central point <10 mm
of septum at an acute angle (<90 )
Septate Presence of uterine septum that that Uniformly convex or with indentation
completely divides cavity from <10 mm
fundus to cervix
Bicornuate Two well-formed uterine cornua Fundal indentation >10 mm dividing
the two cornua
Unicornuate with or without Single well-formed uterine cavity with
rudimentary horn a single interstitial portion of
Fallopian tube and concave fundal
contour
Ghi. 3D ultrasound in M€
ullerian anomalies. Fertil Steril 2009.

ultrasound scan. The remaining 284 women agreed to partic- dal indentation of the endometrial cavity were demonstrated
ipate in the study protocol. The median age of the patients on the coronal plane. In these cases, the fundal indentation at
was 34 years (range, 26–44), and their ethnicity was distrib- the central point appeared as an obtuse angle (Fig. 2C).
uted as follows: Caucasian, n ¼ 272 (95.8%); Afrocaribbean,
After volume ultrasound, office hysteroscopy was per-
n ¼ 10 (3.5%); and Asian n ¼ 2 (0.7%).
formed in the 230 (81%) patients with negative ultrasound
The quality of volume ultrasound was satisfactory in all findings, and combined hysteroscopy-laparoscopy under
cases. Offline analysis of uterine morphology was success- general anesthesia was carried out in the 54 (19%) cases
fully carried out within 5 minutes in each case. A normal uter- with a M€ullerian anomaly suspected at ultrasound. The diag-
ine cavity was demonstrated at ultrasound in 230 (81%) nostic accuracy of 3D ultrasound is summarized in Table 2.
patients, whereas a specific diagnosis of uterine anomaly All women with negative ultrasound findings showed normal
was sonographically performed in 54 cases (19%). Unicorn- uterine cavity at office hysteroscopy. A complete list of the 54
uate uterus (one case) was sonographically diagnosed when abnormal cases detected at ultrasound with the volume ultra-
an asymmetric laterally deviated uterine corpus of tubular sound diagnosis and corresponding findings subsequently
shape with an accessory noncommunicating rudimental achieved at endoscopy is provided in the table. At endoscopy,
horn was demonstrated on the coronal plane. A single tubal the presence of a M€ullerian anomaly was confirmed in all
ostium was detectable on this section. Bicornuate uterus (n cases. Exact concordance between ultrasound and endoscopy
¼ 9) was sonographically diagnosed when two separated around the type of anomaly was verified in 52 cases, includ-
uterine cornua with external fundal indentation R10 mm di- ing all those with septate uterus (partial and complete) and
viding the cornua were demonstrated on the coronal plane two out of three with bicornuate uterus. Ultrasound diagnosis
(Fig. 2A). proved inaccurate in two cases, including an arcuate and a bi-
cornuate uterus that at endoscopy were, respectively, classi-
Septate uterus (n ¼ 35) was sonographically diagnosed
fied as a subseptate and a complete septate uterus.
when a septum dividing the endometrial cavity was demon-
strated on the coronal plane and the external uterine surface
was normal or showed a sagittal notch of <1 cm (Fig. 2B). DISCUSSION
Septate uterus was further classified as complete (n ¼ 14) Our data seem to confirm in a large series of cases that in a se-
or incomplete (subseptate uterus, n ¼ 21) as far as the septum lected group of patients volume transvaginal ultrasound is ex-
itself bridged or did not bridge the fundus to the internal os of tremely accurate for the diagnosis and classification of
the uterine cervix. In subseptate uterus, the fundal indentation congenital uterine anomalies. All women sonographically
at the central point of the septum appeared as an acute angle classified as normal in fact showed no evidence of M€ ullerian
(Fig. 2D). Arcuate uterus (n ¼ 9) was sonographically diag- anomaly at office hysteroscopy. On the other hand, in all pa-
nosed when normal external uterine contour and concave fun- tients sonographically classified as abnormal, a M€ ullerian

810 Ghi et al. 3D ultrasound in M€ullerian anomalies Vol. 92, No. 2, August 2009
FIGURE 2
(A) Rendered image of a bicornuate uterus at volume ultrasound: on the coronal plane, two divergent cornua
divided by a sagittal cleft >10 mm (arrow) are noted. (B) Rendered image of a septate uterus at volume
ultrasound: on the coronal plane, a septum dividing the endometrial cavity and extending to the cervix with
a normal external uterine surface is demonstrated. (C) Rendered image of an arcuate uterus at volume
ultrasound: on the coronal plane, normal external uterine contour and concave fundal indentation of the
endometrial cavity at obtuse angle are demonstrated. (D) Rendered image of a subseptate uterus at volume
ultrasound: on the coronal plane, the septum is noted not to extend to the cervix, and fundal indentation at its
central point appears as an acute angle.

Ghi. 3D ultrasound in M€
ullerian anomalies. Fertil Steril 2009.

anomaly was subsequently confirmed at combined hystero- ative predictive value (100%) registered in this series, volume
scopy-laparoscopy. Furthermore, volume ultrasound proved ultrasound may be proposed as an accurate tool for detecting
highly valuable in suggesting the type of uterine anomaly, uterine anomalies in high-risk patients such as those with re-
as ultrasound classification was endoscopically confirmed current abortion. In this group, the option of office hystero-
in 52 out of 54 abnormal cases (92.3%). scopy has traditionally been considered as a mandatory step
for uterine cavity assessment (12). Being an invasive tech-
Adequate ultrasound imaging of the uterine cavity was ob-
nique, however, hysteroscopy may cause some discomfort
tained within a few minutes in all cases. According to other
to the patient, and even performed by expert hands, it is cer-
investigators (11), all women with concurrent uterine abnor-
tainly more unpleasant than ultrasound for the patient.
malities such as polyps or fibroids were excluded from the
study group, so that only the effect of a malformation on According to our data, in women with negative ultra-
the uterine cavity morphology was subjected to ultrasound sound findings, indication for hysteroscopy certainly
evaluation. Owing to the excellent positive (96.3%) and neg- becomes debatable, as it does not seem to improve the

Fertility and Sterility 811


TABLE 2
Comparison between ultrasound and endoscopic findings in the study group.
Confirmed findings Different findings
Ultrasound diagnosis n at endoscopy at endoscopy
Normal uterus 230 230 —
Unicornuate uterus 1 1 —
Bicornuate uterus 9 8 1 (septate uterus)
Septate uterus 14 14 —
Subseptate uterus 21 21 —
Arcuate uterus 9 8 1 (subseptate uterus)
Ghi. 3D ultrasound in M€
ullerian anomalies. Fertil Steril 2009.

sensitivity of volume ultrasound in detecting uterine anom- patient. However, ultrasound impression of arcuate uterus
alies. On the other hand, because of the high precision of has been possibly favored by the presence of synechiae at
volume ultrasound in characterizing uterine anomalies, the level of tubal ostia due to repeated uterine curettages.
women diagnosed with a specific malformation that may Before metroplasty, synechiae have been hysteroscopically
be treated by means of resectoscope may be conveniently removed, and this has permitted a more reliable evaluation
addressed to an operative hysteroscopy rather than to a diag- of fundal indentation.
nostic endoscopic step. Owing to the high accuracy of 3D
ultrasound for the diagnosis of bicornuate uterus, patients The use of volume ultrasound in the noninvasive diagnosis
diagnosed with this condition can avoid further diagnostic of uterine anomalies has been previously suggested. Most
steps, as operative hysteroscopy is not useful for treating relevant studies have compared the accuracy of 3D ultrasound
such an abnormality. to laparoscopy supported by hysterosalpingography (13)
or hysteroscopy (14), showing a high agreement between
As mentioned above, in two of our cases, 3D ultrasound di- the different techniques. On the other hand, as demonstrated
agnosis proved to be inaccurate, and a specific comment on by other investigators (15), compared with conventional
that is certainly required. In the first case, a woman with ul- two-dimensional ultrasound, volume ultrasound has a higher
trasound suspicion of bicornuate uterus was endoscopically specificity in detecting uterine anomalies. Furthermore, as
diagnosed as having a complete septate uterus. This is cer- reported by other investigators, the reproducibility of 3D
tainly a major mistake, but it was made at the beginning of ultrasound in the diagnosis and classification of congenital
the study when experience in volume reconstruction was still uterine anomalies is extremely high (16).
limited. The same volume data set has been subsequently
reassessed by the same operator, and performing a volume In our study, all women were submitted at least to office
reconstruction of the uterus on a different plane led to the cor- hysteroscopy, which is considered the most valuable method
rect ultrasound picture of a septate uterus. We believe that to detect congenital anomalies of the uterine cavity (12). How-
misdiagnosis was due to an incorrect angle of scrolling ever, a combined hysteroscopic and laparoscopic evaluation
through the uterine fundus. In fact, if the section cut through has been proposed for all cases with abnormal findings at
the fundus of a septate uterus is not perpendicular to that due ultrasound. This policy has been judged reasonable to achieve
to an excessive rotation of the volume, a false impression of in a single step the final diagnosis and, when indicated, the
a cleft in the fundal contour compatible with the diagnosis of appropriate treatment. Some M€ullerian anomalies such as
bicornuate uterus may be raised. The use of a combination of bicornuate or septate uterus in fact are not amenable to be dif-
rendered and mutiplanar images in interpreting the pictures ferentiated at hysteroscopy only and may be confidently clas-
should make the differential diagnosis between the two sified when laparoscopic view of the fundus is simultaneously
conditions more accurate. available. Furthermore, when the diagnosis of uterine anoma-
lies that may benefit from metroplasty is laparoscopically
In the second case, ultrasound diagnosis of arcuate uterus ascertained, under the external control of the fundus, resecto-
was endoscopically changed to subseptate uterus. This is scopic surgery may be more safely undertaken.
a mild inaccuracy as a certain variability in distinguishing be-
tween these two forms of uterine anomalies is not uncommon As shown by our series, M€ullerian anomalies may be de-
even among experienced endoscopists because the diagnosis tected and correctly classified by volume ultrasound thanks
is based on subjective impression rather than on objective cri- to its ability to provide a simultaneous reconstructed view
teria. Furthermore, as far as the clinical management is con- of the internal and external surface of the uterus itself on
cerned, patients with both arcuate and subseptate uteri with the coronal plane. On this basis, women may be treated
a history of recurrent miscarriage are usually treated by with a combined laparoscopic-hysteroscopic approach only
means of resectoscopic metroplasty, as was the case for our when a curative step is clinically indicated and not for

812 Ghi et al. 3D ultrasound in M€ullerian anomalies Vol. 92, No. 2, August 2009
diagnostic purposes as previously recommended. Further- 6. Grimbizis G, Camus M, Clasen K, Tournaye H, De Munck L, Devroey P.
more, in cases with septate uterus undergoing metroplasty, Hysteroscopic septum resection in patients with recurrent abortions and
infertility. Hum Reprod 1998;13:1188–93.
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wall above the septum may be measured by volume ultra- tion of adnexal adhesions, distal tubal occlusion, distal tubal occlusion
sound before surgery to make the resectopic procedure safer. secondary to tubal ligation, tubal pregnancies. Mullerian anomalies
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