Fécamp, France; ** Fellow, TheFetus.net, 2201 Murphy Ave, Ste 203, Nashville, TN37203, USA; Permanent position: Gynecological and Obstetrical Department, CentralMilitaryHospital in Ruzomberok, SlovakRepublic.

[Some images in the second half of this article are no longer available]

Prevalence

The incidence of the uterine malformations is estimated to be between 3 and 4% in the general population. These relatively frequent pathologies are often revealed at the time of the first sonographic examination in early pregnancy. The prevalence of the particular types of the uterine malformations is difficult to estimate. However, the septate uterus seems to be the most frequent anomaly accounting for 30 to 50% of all the cases, followed by the bicornuate uteruses and unicornuate uteruses respectively.

Case report

We report the case of a 22-year-old G1P0 presented her initial ultrasound examination at 6 weeks of gestation. The clinical examination was normal (no vaginal or cervical anomaly was visualized).

Ultrasonography revealed an intrauterine pregnancy with biometry corresponding to the last menstrual date.

6 weeks

Image 1: Developing intrauterine pregnancy (6 weeks of gestation)

An uterine malformation was suspected. The following images represent serial scans from the fundus to the uterine isthmus.

Image 2: Axial section of the uterine fundus with normal external contour of the myometrium. 

Image 3: The two uterine horns separated by a large myometrial layer.

Image 4: Gestational sac in the left horn (note the decreased size of the myometrial layer).

Image 5: Axial section in the subisthmic region (terminal end of uterine septum). Note the thickening of the septum.

Image 6: Longitudinal plane through the uterus showing the interruption of the endometrial line above the isthmus (arrow); CE - cervix; FU - fundus.

Image 7: Power Doppler image showing vascularization of the uterus with hypoechoic poorly vascularized septum.

The images above led us to the diagnosis of the left horn located pregnancy in septate uterus, type Vb (see discussion).

10 weeks

Image 8: Transverse plane through the uterus. The uterine septum is hypoechoic and hypovascular. At this level, the placenta (PL) begins to spread on the posterior wall (retroverted uterus).

12 weeks

Image 9: Longitudinal section of the fetus showing its location belong the uterine septum within the amniotic cavity that had spread to the both uterine horns.

Image 10: The fetal head situated in the right uterine horn.

Embryology

The uterus develops from the two paramesonephric ducts (Mullerian ducts). The caudal two thirds of these ducts give rise to the uterus and the upper third become the Fallopian tubes. The development of the uterus is divided into the three stages:

• 6-9 weeks: the appearance of Müllerian ducts and their caudal midline fusion and connection with urogenital sinus;

• 10-13 weeks: the upward fusion of the caudal parts of the Müllerian ducts;

• 14-18 weeks: the resorption of the medial septum initially separating the caudal parts of the Müllerian ducts to form the utero-vaginal channel as the origin of both uterine cavity and superior 2/3 of the vagina.

The great majority of the uterine malformations can be explained by the failure or arrest of development during these three stages:

• Failure of development of the Müllerian ducts between 6th and 9th week leads to uterine aplasia;

• Failure of Müllerian ducts fusion between 10th and 13th week leads to uterine duplications (uterus didelphys, bicornuate uterus);

• Failure of resorption of the midline septum between 14th and 18th week leads to uterine septation (septate uterus).

Four other important facts:

• As the superior 2/3 of the vagina has the same embryologic origin as the uterus, uterine malformations are often associated with upper vaginal malformations;

• Genital anomalies are often associated with urinary tract anomalies (kidneys, urethra) due to close embryological interactions;

• The independent ovarian and Müllerian ducts development explains the generally normal ovarian morphology and function in the cases of uterovaginal developmental anomalies;

• The uterine malformations are usually not associated with chromosomal or sexual differentiation anomalies.

Classification

The uterine malformations are classified according to the embryologic mechanism leading to their formation. The main classification used in France is the classification of Musset. However, generally accepted is the classification of American Fertility Society (AFS) (1988). Nonetheless, the atypical, or intermediate forms of anomalies are difficult to classify.

Mullerian malformations are divided into four groups:

Imaging of uterine malformations

Sonography

Abdominal and vaginal ultrasonography belong represent the main diagnostic method of uterine anomalies. The most precise investigation of uterine morphology can be done during the second half of menstrual cycle or at the beginning of pregnancy (the thick and echoic endometrium has a better contrast with the adjacent myometrium). 2D sonography allows us to detect many of uterine malformations. However, unicornuate uterus can be missed and discrete forms of septate and bicornuate uterus are not easy to distinguish among themselves. An ideal method of imaging seems to be 3D ultrasonography. The evaluation of the uterine malformations should be accompanied by the renal investigation in effort to find some associated anomalies.

MRI

MRI becomes nowadays the gold standard of the exploration of uterine malformations because it allows a study in several planes and good distinction of myometrium and endometrium. However, access to this examination is still limiting factor in many countries.

Hysterosalpingography

This method is less used currently.

UTERINE ATRESIA OR APLASIA

These anomalies are secondary to partial or complete absence of development of Müllerian ducts. They are frequently associated with renal anomalies.

• Complete bilateral agenesis or complete type I: Rare; incompatible with life because of associated bilateral renal agenesis.

• Incomplete bilateral agenesis or incomplete type I (Mayer-Rokitansky-Küster-Hauser syndrome): The women with this anomaly are infertile because of the absence of functional uterus (two rudimentary uterine horns without cavity are present).
• Unilateral complete agenesis or type II d (also called true unicornuate uterus): This form is characterized by missing of one uterine horn (or the horn is just rudimentary). 2D sonography shows a deviated uterus to one side, but generally the spindle-shaped aspect of the cavity is easier recognized by 3D sonography, MRI or hysterosalpingography.
• Incomplete unilateral agenesia or type II (and subtypes II b and II c): Also called pseudo-unicornuate uterus. This form is much more frequent than the previous ones. In this case the rudimentary horn of variable development is present. The horn can be attached or in some distance from the normal horn. It can be solid or with cavity paved with endometrium. This rudimentary horn can be the seat of an ectopic pregnancy.

The forms above, with rudimentary horn, can be sometime diagnosed by 2D sonography (presence of a horn tissue between the normal hemi-cavity and the contralateral ovary), but 3D sonography or MRI seem to be more precise. The rudimentary horn is generally of small size. Its recognition can be facilitated by the presence of the echoic endometrium inside the horn during the second half of menstrual cycle or at the beginning of pregnancy. In some cases only laparoscopy allows to recognize this condition.

UTERINE DUPLICATIONS

These anomalies are related to defective fusion of the Müllerian ducts. The complete form represents uterus didelphys. The most common form of this group is bicornuate uterus.

• Bicornuate bicervical uterus or type III: This type represents uterus didelphys characterized by the presence of two uterine horns and two cervixes. The vagina can be septated or normal. In addition, this anomaly is occasionally associated with an obstructed hemi-vagina (often with ipsilateral renal agenesis) with consequent hematometry and hematocolpos after the menstruations periods had started.
• Bicornuate unicervical uterus or type IV a or IV b: In this case the uterus consists of one cervix and two divergent horns. A renal aplasia or ectopia can be associated with this anomaly.

The main sonographic feature of the uterine duplications is an invagination of the uterine fundus, well seen on coronal views (or by 3D sonography and MRI). The spacing between the horns with the urinary bladder in the gap between the horns can be recognized as a "V sign" of the bladder. The differential diagnosis can be difficult with a septate uterus when the spacing between the horns is small. The fundal invagination bigger than 1cm of depth and a distinct vascularization on color Doppler images testify the bicornuate uterus.

UTERINE SEPTATIONS

Uterine septations belongs among most frequent uterine malformation. Septations are secondary to the total or partial defect of resorption of the sagittal septum. In this type of malformation the external morphology of the uterus is normal. These anomalies are usually not accompanied by renal anomalies.

• Complete septate uterus or type V a: The septum extends from the uterine fundus to the external os of the cervix. This can imitate duplicity of the cervix. Vagina can be sometime also septated.
• Partial, corporeal, fundal septate uterus or type Vb: In this case the septum is located above the cervix.
• Asymmetric septate uterus: This rare form was described in the Musset"s classification, but is absent in the AFS classification. The uterine body is divided into two asymmetric cavities by a septum going from the uterine fundus to the uterine isthmus. One of the two cavities communicates with the cervix, the other is blind with consequent risk of hematometra, endometriosis or ectopic pregnancy.

In these malformations the external contours of the uterus are normal. On a coronal section the fundal serosa is rectilinear or with mild invagination (less than 1cm). The single uterine cavity is divided by a bridge of fibrous myometrium. The septum is in generally hypovascularized in comparison to the adjacent myometrium.

UTERINE COMMUNICATIONS

These malformations are very rare. The uterus has an isthmic communication between the cavities of the bicornuate or septate uterus. The diagnosis can be done by hysterography or by 3D sonography and MRI.

OBSTETRICAL IMPACTS

The two facts are important to realize:

• More than 50% of women with malformed uterus will stay completely asymptomatic from the obstetrical point of view;
• Anatomical aspect and clinical outcomes can be different and influenced by other, not so striking, associated anomalies like anomalies of endometrium, vascularization, myometrial compliance, cervical competence and others.

Infertility
The prevalence of uterine malformations in the infertile patients is very variable according to all studies, but does not seem to be significantly different from the prevalence observed in the general population. The uterine malformations are not the only factor responsible for the infertility, but it should be taken into account that some of them can increase the risk of a endometriosis. The finding of an uterine malformation must be integrated to the consideration about the obstetrical prognosis.

Early abortions
All uterine malformations can be responsible for early abortions. The frequency of abortions is doubled compared with the women with normal uterus. The incidence of the miscarriages seems to be highest in the case of septate uterus when the trophoblast invades the badly vascularized area of the septum with defective structure of the endometrium.

Ectopic pregnancies
The frequency of the ectopic pregnancies in the cases of malformed uteri does not seem to be different from that found in the general population. Nevertheless, the place of ectopic gravidity is important prognostic factor. When not recognized early, the ectopic pregnancies localized in a rudimentary horn of the unicornuate uteri (type II A or IIB) or asymmetrical septate uteri can lead to serious uterine ruptures.

Late abortions or premature birth
These complications are often secondary to premature rupture of the membranes or to a cervical incompetence and can be associated with all types of uterine malformations.  The rate of childbirth at term in cases of uterine malformations is only 50%. There is also a higher risk of late fetal losses and very premature childbirths.

IUGR
The risk of IUGR appears to be increased in cases of uterine malformation. Some studies described 50% risk of IUGR in the case the unicornuate uterus and some authors found an increase rate of preeclampsia and placental abruption, probably as a consequence of abnormal placentation.

Anomaly of presentation
The risk of abnormal presentation (breech or transverse presentation) is higher in cases of uterine malformations due to mechanical factors that impede normal rotation of the fetus in the uterine cavity.

MANAGEMENT OF UTERINE MALFORMATIONS

Before pregnancy

The management of the uterine malformations before pregnancy comprises the surgical treatment if it is possible and necessary. Some of the malformations remain out of surgical capabilities (unicornuate uterus, didelphys uterus), but surgical procedures can prevent ectopic pregnancy for example in cases of the unicornuate uteri of the type IIa or IIb (excision of the rudimentary horn).

In the bicornuate uteruses type VI, hysteroplastic is theoretically possible in case of symptomatic malformation, but as this malformation is usually more complex, this procedure is done only seldom.

The septate uteri (type V) are the only uterine malformations whose surgical treatment is relatively simple by hysteroscopic excision. This treatment is addressed to the symptomatic patients that had had an obstetrical complication before. However some authors recommend preventive treatment after the anomalies had been diagnosed. Hysteroscopic treatment can be proposed to patients with some types of the bicornuate uteri and arcuate uteri.

However, the two important facts must be taken into account in the surgical treatment of uterine malformations:

• The restoration of normal cavity anatomy is not guarantee of a good obstetrical prognosis (abnormal uterine vascularization, compliance etc.);
• To the contrary with the generally accepted idea, the number of pregnancies doesn"t improve obstetrical prognosis in women with untreated uterine malformations.

During the pregnancy

When the diagnosis of uterine malformation is made at the beginning of pregnancy, the treatment can be only preventive (setting at rest, sonographic monitoring of the fetal growth and the cervical competence). Cervical cerclage should be proposed only in the case of proved cervical incompetence observed in 1/3 to 1/4 of uterine malformations.