The Egyptian Journal of Radiology and Nuclear Medicine (2013) 44, 357–365

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology andNuclearMedicine

www.elsevier.com/locate/ejrnmwww.sciencedirect.com

ORIGINAL ARTICLE

Uterine septum structure and reproductive performance:

Role of 3D TVUS and MRI

Ghada K. Gouhar a,*, Soha Siam b

a Department of Radiodiagnosis, Faculty of Medicine, Zagazig University, Sharkia, Egyptb Department of Obstetrics and Gynecology, Faculty of Medicine, Zagazig University, Sharkia, Egypt

Received 31 December 2012; accepted 19 February 2013Available online 25 March 2013

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KEYWORDS

Three-dimensional transvag-

inal ultrasound examination;

MRI;

Septate uterus

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Abstract Objective: To evaluate the role 3D TVUS and MRI in diagnosing the nature of uterine

septum according to the reproductive performance with histopathological examination as the refer-

ence standard.

Patients and methods: The study included 36 patients in the reproductive age presented with infer-

tility or recurrent pregnancy loss, and diagnosed hysteroscopically with double uterine cavity. All

patients were subjected to 3D TVUS. Cases in which the diagnosis of septate uterus was not con-

firmed by 3DUS were excluded from the study. The remaining 29 patients confirmed to have uterine

septum partial or complete were included. 3D TVUS with VOCAL, was applied in order to calcu-

late the volume of the septum, echostructure and its vascularity index (VI). The patients were then

referred to MRI examination, patients were referred to operative hysteroscopy for hysteroscopic

metroplasty. Sample of septal tissue was obtained and sent for histopathological examination.

Results: The Vascularity index (VI) of the muscular septum (16.63 ± 5.7%) was significantly

higher than the fibrous septum (3.6 ± 1.17%). The sensitivity, specificity, PPV, and NPV in diag-

nosing septate uterus were 100%, 90 %, 95%, and 100% for 3D TVUS, and 95%, 80%, 90%, and

89% for MRI respectively.

Conclusion: 3D TVUS is an accurate, less expensive, and a rapid examination than MRI in diag-

nosing uterine septa structure, it can be considered as the reference standard in diagnosing and

characterizing septate uterus.� 2013 Production and hosting by Elsevier B.V. on behalf of Egyptian Society of Radiology and Nuclear

Medicine. Open access under CC BY-NC-ND license.

10109902.m (G.K. Gouhar).

tian Society of Radiology and

g by Elsevier

ing by Elsevier B.V. on behalf of E

p://dx.doi.org/10.1016/j.ejrnm.2013

1. Introduction

Septate uterus is the most common congenital uterine malfor-

mation, constituting about 55% of all mullerian duct anoma-lies (1). The incidence of congenital uterine anomalies in thegeneral population is 3–4%, which is significantly higher in pa-

tients with reproductive failure (2–4).

gyptian Society of Radiology and Nuclear Medicine.

.02.009

358 G.K. Gouhar, S. Siam

The uterine septum affects female reproductive perfor-mance through infertility, recurrent miscarriages or obstetriccomplications (5).

Fedele et al. 1993, were the first to hypothesize that uterineseptum may affect fertility through hindering implantation.Based on histological samples obtained during operative hys-

teroscopy, septal endometrium showed to be different fromthe endomentrium of the lateral uterine wall regarding: glan-dular ostia number, irregularly scattered decreased ciliated

cells with incomplete ciliogenesis and decreased ciliated tonon- ciliated cell ratio (6).

There is agreement that vascularity within the septum isuncharacteristic. Insufficient vascularization and altered rela-

tionship between the myometrium and endometrial vesselsand nerves, resulting in abnormal placentation, may be thecause of poor reproductive performance (7).

Moreover, clinical studies reported on increased muscle tis-sue contents and uncoordinated contractility of the uterineseptum (8).

Morphologic narrowing of the cavity with subsequentreduction of the endometrial capacity has also been suggestedas a cause of poor outcome (9).

For the evaluation of uterine malformations several meth-ods are available. Regarding the uterine cavity HSG & hyster-oscopy are essentially useful while laparotomy & laparoscopycan be used for evaluation of uterine fundus. MRI and 3DUS

however can combine the study of both these structures. MRIproved in many studies as an excellent tool for diagnosis ofmullerian anomalies (10,11).

3DUS represents a useful alternative, for lower cost & bet-ter tolerance by the patient. It provides images of a very similarquality of those of MRI (12).

There are only few studies comparing both techniques forthe diagnosis of mullerian duct anomalies (13).

To the best of our knowledge no previous studies have com-

pared the accuracy of 3DUS and MRI in diagnosing uterinesepta structure with histologic examination as the goldstandard.

The aim of this study was to evaluate the role 3D TVUS

and MRI in diagnosing the nature of uterine septum accordingto the reproductive performance with histopathological exam-ination as the reference standard.

2. Patient and methods

This study was conducted at the Zagazig university hospital

between October 2009 and September 2012. 36 patients inthe reproductive age presented with infertility or recurrentpregnancy loss diagnosed hysteroscopically with double uter-

ine cavity were recruited. Patients with associated uterine le-sions, (polyp, or fibroids) or with other factors causinginfertility or recurrent pregnancy loss were excluded from thestudy. The study was approved by the local ethics committee

of Zagazig University Hospitals and informed consent was ta-ken from all patients.

All patients were subjected to history taking (Reproductive

history of each patient was recorded), physical examination,2D ultrasound examination, then referred to 3D ultrasound(3DUS). Cases in which the diagnosis of septate uterus was

not confirmed by 3DUS were excluded from the study (twocases diagnosed as arcuate and five patients with bicornuate

uterus). The remaining 29 patients confirmed to have uterineseptum partial or complete were included. 3D TVUS with VO-CAL, was applied in order to calculate the volume of the sep-

tum, echostructure and its vascularity index (VI). The patientswere then referred to MRI examination.

After completing 3D TVUS and MRI examinations, pa-

tients were referred to operative hysteroscopy for hysteroscop-ic metroplasty under laparoscopic guidance. Sample of septaltissue was obtained during the procedure and sent for histopa-

thological examination by an expert pathologist.

2.1. Three-dimensional ultrasound examination

Examinations were performed using MyLab 60 (esaote, Italy)ultrasound machine. All examinations were performed withreal time 4D endocavitary probe BE1123 4–9 MHz. One tothree static volumes of the uterus was obtained transvaginally.

The uterus was initially visualized on 2D ultrasound in a strictmid-sagittal view, then the capture window was adjusted to ob-tain the ideal 3D volume, then color Doppler was activated.

The virtual organ computer aided analysis (VOCAL) imagingprogram was used to calculate septum volume and vascularity.The volume was then achieved using a sweep angle of 95� fromone side of the uterus to the other, bisecting the capture plane.The volumes were manipulated until a satisfactory surface ren-dered image was attained of the fundus, uterine cavity and thecervical canal. When a mid-sagittal plane was used to capture

the volume, the rendering box in capture image was adjustedto include the uterine fundus. When the volume was attainedin a transverse plane, both uterine horns were included in

the rendering box. Thick slice option was used for better visu-alization of the uterine cavity. The vascularization index (VI)was calculated using the VOCAL software, and it is the ratio

of color voxels to all voxels in the region of interest expressedas percentage.

2.2. MRI examination

MR imaging was performed with the use of a 1.5-T MR (Achi-eva, Philips Medical Systems, Netherland B.V.) by using pelvicsurface coil. Patients were positioned in the supine position and

were informed to avoid movement during the examination. Thefollowing sequences were taken: axial T1-weighted images[(400–600/12–15) repetition time msec/echo time msec] ,T2-

weighted fast spin echo images in the sagittal, long-axis, short-axis, and coronal planes of the uterus (2000–4000/90–100) witha section thickness of 2–4 mm, an intersection gap of 0–1 mm,

flip angle 9�, NEX 2, and field of view (FOV) 200–350 mm.Findings were classified according to the The American

Fertility Society (AFS) (14), (complete septum as class Va

and partial septum as class Vb). To discriminate bicornuatefrom septate uteri using 3D ultrasound the formula proposedby Troiano and McCarthy (15) was used: a line was traced,joining both uterine horns. If this line crossed the fundus or

was 65 mm from it, the uterus was considered bicornuate,while if it was >5 mm from the fundus, considered septateuterus, regardless of whether the fundus was smooth, dome-

shaped, or discretely notched (Fig. 1).When differentiating bicornuate from septate uteri using

MRI, cases with fundal incision >1 cm were considered to

be bicornuate uterus.

Fig. 1 Classification criteria for US differentiation of septate from bicornuate uteri. (A) When apex (3) of the fundal external contour

occurs below a straight line between the tubal ostia (1, 2) or, (B) 5 mm (arrow) above it, the uterus is bicornuate. (C) When apex is more

than 5 mm (arrow) above the line, uterus is septate (quoted after Troiano and McCarthy15).

Table 1 Reproductive history of the 29 patients.

Reproductive history No. (%)

Primary infertility 13 (44.82)

RPL (Total) 16 (55.17)

-RPL with no history of term pregnancy 5 (31.25)

-RPL with a history of term pregnancy 11(68.75)

Uterine septum structure and reproductive performance 359

Distinction between septate and arcuate uteri was carried

out in the coronal plane on both 3D ultrasound and MRI.Both types have a normal contour, however, the fundal inden-tation (in uterine cavity) in arcuate uterus appears as an obtuse

angle at the central point (16), with a depth of up to 1.5 cm(17), whereas fundal indentation in septate uterus character-ized by an acute angle at the central point, with a depth of1.5 cm or more.

2.3. Hysteroscopic metroplasty

All patients were referred to hysteroscopic metroplasty, which

was done under laparoscopic guide. Under general anesthesia,Versa Point system (Gynecare Versa Point with resectoscpicknife electrode; Ethicon, Somerville, NJ, USA) was used, with

saline solution used as the distention medium. In an upwarddirection the septum was divided, till both tubal ostia wereequally visible. During the procedure sample of the septa was ta-

ken using punch biopsy forceps avoiding the tip of the septum.The specimens were sent for histopathological examination.

2.4. Histopathological examination

Specimens obtained from the septum were sent for histopa-thology to determine the nature of the septum (myometrial, fi-brous tissue, and the vascularity).

All the biopsy specimens were fixed in 10% saline for 24 h.Washing was done in tap water then serial dilutions of alcoholabsolute (ethyl) were used for dehydration. Specimens were

cleared in xylene embedded in paraffin at 56� in hot air ovenfor 24 h. Paraffin bee wax tissue blocks were prepared for sec-tioning at 4 lm thicknesses by slidge microtome. The obtainedtissue sections were collected on glass slides, deparaffinized

and stained by hematoxylin and eosin stain and Masson’s tri-chrome then examined by light microscope (18).

2.5. Statistical analysis

Data were analyzed using a specialized software (SPSS forWindows v10). The sensitivities, specificities, positive predic-

tive values (PPV), negative predictive values (NPV) and accu-racies of the two imaging techniques in diagnosing anddetermining the nature of uterine septum, with the histopathol-

ogical examination of the excised specimens as standard of ref-erence were calculated. Student’s t-test was used to represent

the relation between the vascularity index (VI) and the type

of septum. A P-value < 0.05 was considered significant.

3. Results

Between October 2009 and September 2012, 36 patients in thereproductive age (26 ± 3.2) that presented with reproductivefailure whose hysteroscopic examinations showed double uter-

ine cavity, were referred to 3D TVUS. Five patients (12.8%)were diagnosed as bicornuate uterus, and two patients(5.1%) with arcuate uterus, the remaining 29 with septateuterus, were included in the study and were examined by both

3D TVUS and MRI examination. Of the 29 patients studied 13patients had primary infertility and 16 patients had recurrentpregnancy loss (RPL) (Table 1).

Among 29 cases with septate uterus, 18 cases had partialseptum (class Vb) and 11 had complete septum (classVa). His-tology of the septum showed myometrial tissue with normal

vascularization (muscular septum) in 19 patients, and promi-nent fibrous tissue with poor vascularization (fibrous septum)in 10 patients. On MRI 18/19 cases were correctly diagnosed

as muscular septum as the septum showed isointense signalto the myometrium, (one case had lower signal intensity thanthe surrounding myometrium and was incorrectly diagnosedas fibrous septum). 8/10 cases were correctly diagnosed as fi-

brous septum and displayed lower signal intensity than the sur-rounding myometrium (Two cases had isointense signal to thesurrounding myometrium and were incorrectly diagnosed as

muscular septa).On 3D TVUS 19/19 cases were correctly diagnosed as mus-

cular septum, and showed significantly higher vascularity in-

dex (VI) (16.63 ± 5.7%) than the fibrous septum(3.6 ± 1.17%) that was correctly diagnosed in 9/10 patients(t-test 7.08, and P < 0.0001).

Studying the relation of these data to reproductive history

showed that patients with recurrent pregnancy loss (RPL)

Table 2 Sensitivity, specificity, PPV, and NPV of 3D TVUS

and MRI in diagnosing septate uterus.

Sensitivity

(%)

Specificity

(%)

Positive

predictive

value (%)

Negative

predictive

value (%)

Kappa

test

P

value

3D TVUS 100 90 95 100 0.92 <0.0001

MRI 95 80 90 89 0.76 <0.0001

360 G.K. Gouhar, S. Siam

had higher vascularization index (muscular septum) than thosewith a history of infertility (fibrous septum) (12.43 ± 1.2 vs.4.14 ± 1.1).

The mean values ± standard deviation of (VI) in the exam-ined 29 cases is shown in (Fig. 2).

With the histological examination as the gold standard, the

sensitivity, specificity, PPV, and NPV in diagnosing septateuterus were 100%, 90 %, 95%, and 100% (kappa 0.92, andP < 0.0001) for 3D TVUS, and 95%, 80%, 90%, and 89%

(kappa 0.76, and P < 0.0001) for MRI respectively (Table 2).Representative cases are shown in (Figs. 3–6).

4. Discussion

The septate uterus is accompanied with some of the poorestreproductive outcomes which have been shown to improve

after hysteroscopic metroplasty (19–22).The prevalence of septa in patients who have had recurrent

pregnancy loss is well known, with reported spontaneous abor-tion rates from 26% to 94%. (23–28) The etiology of reproduc-

tive failure in those patients was traditionally related to thefibrous and avascular nature of the septum, (7,29).

The connective tissue of the septa is thought to result in

poor decidualization and placentation at the site of implanta-tion. There is controversy about the amount of fibrous tissue.Fayez et al., (7) found more connective tissues (CT) and less

muscle fibers while Dabirashrafi et al., (30) stated that the sep-tum composed of more muscles and less CT. Results presentedby Kupesic and Kurjak (31) demonstrate that patients withvascularized septa had a significantly higher rate of obstetrical

complications than those with avascularized septa. They pos-tulate that obstetrical complications are caused by the higherand uncoordinated activity of muscular tissue.

3D TVUS is a relatively new technique which allows theuser to acquire the coronal or face-on view of the uterus. Thisview depicts both the serosal surface of the fundus and endo-

metrial cavity which is useful to differentiate some varietiesof MDAs as bicornuate, unicornuate and septate. (32).

There are a few studies (31,33,34) which evaluated the accu-

racy of 3D US in the diagnosis of septate uteri. The range oftheir results was: sensitivity (98.38–99.27%), specificity (100–100%), positive predictive value (100–100%) and negative pre-

Fig. 2 The mean values ± standard deviation of (VI) in the

examined 29 cases.

dictive value (96–97.61%) and overall accuracy (99.44–100%)of 3D US in diagnosing and differentiating uterine septum

from other types of MDAs.In a study of Exacoustos1 et al., (35) 16 patients with sep-

tate uterus were examined by 3D TVS where, septal length,

width, volume, echostructure and vascularization index (VI),were evaluated. During hysteroscopic removal of the uterineseptum, specimens of the septum were obtained for histologi-

cal evaluation. Histology of the septum showed more connec-tive tissues and few vessels in six cases and normalmyometrium and vessels with a thick muscle wall in 10 cases.3D TVS of septa with myometrium content showed VI of

the septum (12.6 ± 2.7%) significantly, higher compared tothose with fibrotic septa (VI 4.3 ± 3.2%).

In another study of Exacoustos1 et al., (36) sixty-five pa-

tients diagnosed with septate uterus were examined with 3DUS. Histology of the septum showed poor vessels in nine pa-tients, and normal vessel amount in 11 cases, the VI

(17.49 ± 8.4%) was significantly higher than the nine caseswith poor vessel amount ‘‘fibrotic septa’’ (1.83 ± 1.26%).

In a study of Gaafar et al., (37), Twenty-two women withuterine septa were subjected to 3D power Doppler (3D TVUS)

with VOCAL to calculate septum volume and vascularity in-dex (VI), there was a significant positive correlation betweenthe septum VI and the percentage of myometrial content on

histological examination.In this study, histology of the septum showed myometrium

tissue with normal vascularization (muscular septum) in 19 pa-

tients, and prominent fibrous tissue with poor vascularization(fibrous septum) in 10 patients. On 3D TVUS 19/19 cases werecorrectly diagnosed as muscular septum, and showed signifi-

cantly higher vascularity index (VI) (16.63 ± 5.7%) than thefibrous septum (3.6 ± 1.17%) that was correctly diagnosedin 9/10 patients (t-test 7.08, and P < 0.0001).The relation ofthese data to reproductive history showed that patients with

RPL had higher vascularization index (muscular septum) thanthose with a history of infertility (12.43 ± 1.2 vs. 4.14 ± 1.1).

Using histological examination as the gold standard, the

sensitivity, specificity, PPV, and NPV in diagnosing and char-acterizing septate uterus were 100%, 90%, 95%, and 100%(kappa 0.92, and P < 0.0001) for 3D TVUS.

MRI has emerged as an excellent technique for evaluationof MDAs (1,38,39). It permits the physician to evaluate boththe uterine fundus & cavity. Therefore, several authors argue

that MRI should be considered as the new reference standardfor MDA evaluation (1,10,40,41).

Only a few published studies (10,34,42,43) have evaluatedthe efficacy of MRI for MDA evaluation. The Sensitivity

was from 28.6% to 100%, and specificity from 100% to

Fig. 3 Three-dimensional surface rendered ultrasound image (a–c), and MRI (d–f) showing: flat outer uterine contour, and the fundal

indentation has an acute angle at the central point, >1.5 cm deep (D3 = 3.02 cm) and the line joining both horns is >.5 mm from the

fundus (D2 = 0.79 cm) (a, b), 3D of the blood flow within the septum with a VI of 8.7% (c). T2-weighted fast spin-echo images (d–f), long-

axis of the uterus and cervix (d), and long-axis of the uterus (e), and coronal views (f), showing flat outer fundal contour, and the

myometrial septum (isointense to the myometrium), A photomicrograph of the excised uterine septum specimen showing smooth muscle

content (g).

Uterine septum structure and reproductive performance 361

100% in diagnosis of septate uterus, with an overall accuracy

of 100%.With the initiation of pelvic MR imaging, it was perceived

that the signal intensity of the septum was usually myometrial

(i.e., isointense to myometrium) (10,44). Although the majorityof septa contain myometrium in their upper regions, MRI stillcan differentiate a septum from myometrium by the different

signal intensities attained from each. In terms of intensity,myometrium is the reference, isosignal intensity indicatingmuscle and low signal intensity indicating fibrous tissue (13).

In a study of, Zreik et al., (45) MR signal intensity of theseptum was evaluated along with pathologic specimens, allpartial septa contained myometrium, whereas patients withcomplete septa had evidence of myometrium in the upper seg-

ment of the septum and fibrous tissue in the lower segment.In this study,MRI correctly diagnosed 18/19 cases asmuscu-

lar septum, where the septa showed isointense signal to themyo-

metrium (19 cases were diagnosed histologically as muscular

septum), and 8/10 cases were correctly diagnosed as fibrous sep-

tum and displayed lower signal intensity than the surroundingmyometrium (10 cases were diagnosed histologically as fibrousseptum).

Using histological examination as the gold standard, thesensitivity, specificity, PPV, and NPV for MRI in diagnosingand characterizing septate uterus were 95%, 80%, 90%, and

89% (kappa 0.76, and P < 0.0001).Although MRI may provide a better impression of the

pelvic anatomy and associated renal anomalies, 3D ultra-

sound has the advantage over MRI as it is less expensiveand better tolerated by patients (13). 3D ultrasound aidedus to make measurements of the septum such as lengthand thickness. The volume of the cavity can be calculated

as well as the study of septal vascularization, which can af-fect fertility prognosis, thus helping the choice of treatment(46–48). As 3D US becomes more common and as physi-

cians become more skilled in evaluating uterine volumes,

Fig. 4 Three-dimensional surface rendered ultrasound image (a, b), and MRI (c, d) showing: flat external uterine contour and the blood

flow within the upper part of the septum with a VI of 1.2% (a, b). T2-weighted fast spin-echo images (c, d), long-axis of the uterus (c), and

coronal at upper septal level (d), showing prominent upper myometrial component (isointense to the myometrium) and small lower fibrous

component (hypointense than the myometrium).

Fig. 5 Three-dimensional surface rendered ultrasound image (a), and MRI (b–d) showing: flat external uterine contour and the fundal

indentation has an acute angle at the central point, >1.5 cm deep (D3 = 1.92 cm) (a). T2-weighted fast spin-echo images (b–d), long-axis

of the uterus (b), short-axis at lower septal level (c), and short-axis at level of uterine cervix (d), showing the septum with prominent upper

myometrial component (isointense to the myometrium) and small lower fibrous component (hypointense than the myometrium) (b, c), the

low-signal longitudinal structure seen in (d) corresponding to the normal cervical mucosal folds.

362 G.K. Gouhar, S. Siam

Fig. 6 Three-dimensional surface rendered ultrasound image (a–c), and MRI (d, e) showing: normal external uterine contour and the

fundal indentation has an acute angle at the central point, >1.5 cm deep (D3 = 1.52 cm), and the line joining both horns is >.5 mm from

the fundus (D2 = 0.56 cm) (a, b), no blood flow seen within the septum with a VI of 0.25% (c). T2-weighted fast spin-echo images (d, e),

long-axis (d), and short-axis (e), showing fibrous septum of low-signal intensity (hypointense than the myometrium).

Uterine septum structure and reproductive performance 363

3D US will be the reference standard for the diagnosis ofMDAs (49). 3D US is no longer operator-dependent andthe 3D volume is generated by the automatic sweep of the

mechanical transducer (47).Few studies have compared MRI and 3D US in MDAs,

Bermejo et al., (13) stated that, there were high degrees of con-

cordance between 3-D US and MRI (kappa index: 0.878 (95%CI, 0.775–0.980)] in the diagnosis of MDAs. However, in an-other study, Faivre et al., (50) showed that 3D TVS appearsto be extremely more accurate than MRI for the diagnosis

and differentiating septate and bicornuate uterus.In conclusion, 3D TVUS is an accurate, less expensive, and

a rapid examination than MRI in diagnosing uterine septa

structure, it can be considered as the reference standard indiagnosing and characterizing septate uterus.

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