Congenital Malformations of
Uterus and Reproduction

Pankaj Desai, Sameer Dixit


Developmental abnormalities of the Müllerian system are one of the most fascinating conditions in gynecology. A wide range of abnormalities occur, ranging from mild to severe. Müllerian abnormalities are associated with renal and axial skeletal abnormalities and management also involves investigations and treatment of these conditions.
The earliest reported case of Müllerian abnormality is in 16th century.1 The actual incidence of the Müllerian abnormalities is unknown. The true incidence may never be known as these are grossly under reported in childhood and over reported in the population undergoing infertility treatment. The incidence varies widely and depends on the type of study. Most authors report an incidence varying from 0.1–3.5 percent. The most accepted incidence is 4.3 percent for a general population and fertile women, 3.5 percent for infertile women and 13 percent in women with recurrent pregnancy loss.2 In a study of women undergoing Müllerian assessment at the time of undergoing tubal ligation, an incidence of 3.2 percent was identified.3

The incidence also varies with the type of diagnostic test used. In a study4 of women undergoing HSG for recurrent pregnancy loss, the incidence was 8–10 percent. With emergence of more sensitive diagnostic tests, standardized classification and aggressive management, a more realistic incidence of the abnormalities would emerge in future.

The reproductive organs of a woman consist of the external genitalia, the Müllerian tubes and the gonads. All three develop from different primordial origins and in close association with the urinary system and the hind gut. In women, the Müllerian system develops over the Wolffian system. The cranial parts of the Wolffian system persist as epoophoron and the caudal parts as the Gartner’s duct. The Müllerian system persists and forms the adult fallopian tubes, the uterine corpus, the cervix and part of the vagina.

At 37 weeks after fertilization, the Müllerian ducts appear on either side of the Wolffian duct as invagination of the dorsal celomic epithelium. The site of the origin remains patent as the fimbrial end of the Fallopian tubes. The paired Müllerian tubes grow caudally and medially until they meet together in the midline and become fused together. They then converge on the urogenital septum.

The solid Müllerian tubes undergo simultaneous canalization to form the tubular structures. The cranial parts which remain patent and separate evolve into the Fallopian tubes. The upper fused portions of the tubes form the uterus while the lowermost fused portion forms the cervix. The vagina is formed from both the lower end of the fused Müllerian ducts and the urogenital sinus. The mesenchyme surrounding the Müllerian ducts condenses to form the musculature of the female genital tract.

Congenital abnormalities of the female genital tract occur due to errors in this developmental process.5 These include:
• Agenesis/Hypoplasia
• Abnormal fusion with urogenital sinus
• Abnormal lateral fusion of the paired Müllerian tubes
• Abnormal resorption of the septum of the fused Müllerian tubes
Developing kidney and urinary system closely follows Müllerian system. So, their abnormalities are closely associated with abnormalities of Müllerian system. Disruption of developing local mesoderm and somites accounts for some axial skeletal abnormalities. Cardiac and auditory defects are occasionally associated. Ovarian morphogenesis is distinct from Müllerian organogenesis. Hence, in these conditions, the ovarian function and hormonal milieu is normal.

The abnormalities occur due to disruption of the morphogenesis. Various factors6 have been implicated in this. These include:
1. Abnormal intrauterine milieu
2. Teratogens like DES and Thalidomide
3. Genetic factors

Genetic factors involved are complex. They commonly occur sporadically. If familial incidence is detected then it is usually multifactorial. Other modalities of inheritance like autosomal dominant, autosomal recessive and X-linked disorders also exist.6 Müllerian anomalies may also represent a part of the multiple malformation syndromes.7

Associated anomalies are usually seen in cases of Müllerian aplasia (AFS class I). Associated urological anomalies range between 15–40% in these cases and skeletal anomalies (congenital absence or fusion of vertebrae) occur in 12–50% of these cases.8 An association between MRKH syndrome and Klippel-Fiel syndrome is reported. This syndrome is characterized by congenital fusion of the cervical vertebrae, a short neck, low posterior hairline and limited range of motion in cervical spine.9 The MURCS association (Müllerian duct aplasia, Unilateral Renal aplasia, Cervicothoracic Somite dysplasia) is another variant. Infrequently auditory deficits and cardiac defects can be found. The karyotype of the females having Müllerian aplasia is 46 XX.

Müllerian agenesis has been associated with variants of galactose-1-phosphate uridyltransferase (GALT) enzyme. This finding suggests that increased exposure to galactose is responsible for abnormal Müllerian development.10
Other theories about genetic disorders include abnormalities in MIS (Müllerian Inhibitory Substance) gene, loss of function mutation in WNT4 gene and abnormalities of HOXA9-HOXA13 genes. However, none of these have been consistently associated.

In case of MRKH syndrome, the patient may present with primary amenorrhea. In cases of a bicornuate uterus, patient may complain of dysmenorrhea. In cases of a vertical vaginal septum, the patient may come with the complaint that a tampon is unable to stop menstrual flow. In case of an obstructive vaginal septum, the patient may complain of dyspareunia.

Clinical Examination
Per speculum examination may reveal vaginal septum or duplication of cervix. Bimanual examination may help in identifying another horn.

This has been the classical tool for diagnosis of the uterine anomalies (Figure 1). When the classic picture of the uterus with two fallopian tubes is seen, Müllerian abnormalities are almost ruled out.

Figure 1 HSG image of bicornuate uterus

Standard Sonography

In routine sonography, the key structure to be scrutinized is the endometrial cavity. In a normal uterus, the endometrial cavity is single. In a bicornuate uterus, two cavities are appreciated (Figure 2). It must be noted that it is difficult to appreciate two cavities in a longitudinal scan. However, the clinching image is the transverse plane. The two uterine cavities in a cross section are easily identified. A TV sonography gives better diagnosis than the TA sonography. The advantages of sonography are that it is easily available; it is widely acceptable to the patients and is relatively cheap. However, the drawbacks are that the intracavitary lesions are not easily identified, a septum is not appreciated well and it does not depict the external contour of the fundus.

Figure 2 Bicornuate uterus

Saline Infusion Sonography (SIS)

SIS combines the USG with HSG. A catheter is placed inside the endometrial cavity and saline is instilled to achieve separation of the walls of the endometrial cavity along with continuous transvaginal ultrasound visualization. It is usually performed within first 10 days of the cycle. It is not performed after that period, firstly to avoid aborting an early pregnancy and secondly, the thick secretary endometrium may appear wrinkled to give false positive impression of endometrial pathology.

A balloon catheter like the pediatric Foley’s is inserted with tip within the uterine cavity. The balloon is distended with 1ml of water to prevent backflow of the saline. Slow instillation of 3 to 10 ml of prewarmed saline is done. Imaging with transvaginal sonography is done to visualize separation of the uterine walls (Figure 3). Once adequate distension is confirmed, a sagittal sweep from cornu to cornu and an axial sweep from fundus to the cervix are done. The balloon is then deflated and fluid allowed to flow out. A second examination with empty uterus is performed. At the end of the examination, free fluid in the pouch of Douglas is looked for. Its presence denotes patency of at least one fallopian tube.
Potential pitfalls include blood clots or mucous plugs (created by shearing effect of the catheter) being mistaken for intrauterine pathology or overdistension of the uterus causing intrauterine pathology to be missed.

Figure 3 SIS showing uterine cavity

3 Dimensional Sonography
Conventional 3D sonography or 3D sonography coupled with saline infusion is better than 2D sonography (Figures 4 to 6). It involves rapid acquisition of data volumes which are stored for subsequent analysis. Acquisition of the coronal plane improves diagnosis in almost 30.8 percent of the patients.11 This includes better evaluation of the external uterine contour, detection of adhesions and identification of intrauterine pathologies.

Figures 4A to D Multiplanar rendering of 3D acquisition showing all three planes

Figure 5 A 3D rendered image. Outer arrows point to the fundus, inner arrows to endometrial cavity and single arrow to the catheter tip

Figures 6A to D 3D Sonography

Laparoscopy allows one to see the fundus of the uterus from outside. The differentiation between the bicornuate uterus and the septate uterus is made by the appearance of the fundus. A septate uterus shows single convex fundus while a bicornuate uterus shows two cornuae.

Figures 7 to 9 show Helical CT image of normal uterus, CT image of bicornuate uterus with horse-shoe kidney, MRI image of bicornuate uterus and hysteroscopic image of subseptate uterus respectively.

Figures 7 Helical CT image of normal uterus

Figures 8a and B CT image of bicornuate uterus (A) with horse-shoe kidney (B)

Figure 9 MRI image of bicornuate uterus

ESHRE/ESGE consensus on diagnosis of female genital anomalies (21)

Diagnostic Methods:

1. Clinical examination- An essential starting point and essential part of the evaluation. It also offers unique evaluation of vaginal and cervical abnormalities
2. HSG- It offers reliable information regarding uterine anatomy in the absence of cervical obstruction. It can also provide information regarding cervical can if it is patent. It however, does not provide any information regarding anatomy of vagina. It can not be used for diagnosing obstructive abnormalities. Its efficacy is limited by false positive and false negatives
3. 2D USG- It is a reliable, objective and measurable tool. Its an essential part of the assessment. However, it is dynamic, depends on experience of the clinician. It needs a systematic approach.
4. Recommendations for proper use of 2D USG- The endometrial line should always be visible for precise imaging of the uterus. Serial sagittal and transverse scan should be taken extending beyond the margins of the uterus.
5. Hysterosalpingo contrast sonography- Early follicular phase is recommended to avoid pregnancy and artefacts due to thick secretary endometrium.
6. 3D USG- It can provide highly reliable, objective and, most importantly, measurable information for the anatomy of the cervix, uterine cavity, uterine wall, external contour of the uterus and for associated pelvic pathology; the coronal plane of the uterus does provide a clear image of the cavity and the external profile of the uterine fundus. 3D volumes give reliable and objective representation of the examined organs more independently of the examiner overcoming the limitations of obtaining coronal images with 2D sonography. It can provide, also, measurable information even for obstructed parts of the female genital tract.
7. Recommendations for proper use of 3D USG- This method should be started with a 2D evaluation of the uterus. Use in mid cycle or luteal phase is encouraged as this demonstrates the endometrial wall and the outline of the cavity at its best. Contrast medium could be used for the evaluation of the cavity and the tubes; in these cases, the examination has to be performed in the early follicular phase. Save a 3D volume for off-line analysis. The reconstructed coronal plane of the uterus might show the cavity and the external uterine profile as well as the tubal angle and the junctional zone, if possible along all the endometrium and cavity. Acquisition of an isolated cervical volume, without including the uterus: from a mid-sagittal plane, an axial plane of cervix can be obtained in 80 % and a coronal plane in 20 %of the cases; in cases of uterine malformations, the extent of the cervix and the limits of the cervical canal may be studied better.Diagnosis of associated vaginal anomalies can be done by trans perineal acquisition of the pelvic floor volume after filling the vagina with gel or saline; an axial plane can be obtained from a mid-sagittal plane.
8. MRI- It is non-invasive and it has no radiation. It gives a reliable and objective representation of the examining organs in the sagittal, transverse and coronal plane (three dimensions). It can be used for diagnosis in cases of complex and obstructing anomalies. Electronic storage of the diagnostic procedure is, nowadays, routinely done for re-evaluation.
9. Hysteroscopy- It is minimally invasive giving the additional opportunity of treating T-shaped, septate and bicorporeal septate uterus. Its objective includes estimation of the cervical canal and endometrial cavity (differential diagnosis of T-shaped and infantile uterus). It provides a minimal invasive evaluation of the vagina and/or cervix in case of virgo. Electronic storage of the procedure is, nowadays, routinely done for re-evaluation.
10. Endoscopy; laparoscopy and hysteroscopy- It provides highly reliable information for the anatomical status of the vagina (vaginoscopic approach), cervical canal, uterine cavity, tubal ostia, external contour of the uterus and the intra- peritoneal structures.
11. The invasiveness of the laparoscopic approach makes it not acceptable as a first-line screening procedure; it complements indirect imaging in the diagnosis of more complex anomalies in combination with possible surgical actions. It offers supplementary information about partial or total absence of Fallopian tubes and abnormal localisation of ovaries.
12. Highest degrees of overall diagnostic accuracy were in de-creasing order: 3D US (97.6 %), sonohysterography (SHG; 96.5 %), 2D US (86.6) and hysterosalpingography (HSG; 86.9 %). MRI was shown to be able to correctly subclassifiy 85.8% of anomalies. Overall, it appears that 3D US may be more accurate than MRI in sub-classifying malformations, although it should be noted that sub-classification is hindered due to the subjective nature of the previous classifications adopted.

Uterine wall thickness:

1. Uterine wall thickness is an important parameter and a reference point for the definitions of dysmorphic T- shaped, septate and bicorporeal uteri according to the new classification system. The adoption of an objective criterion for the definition of uterine deformity is one of the advantages of the new classification system since according to AFS classification the detection of anomalies was based only on the subjective impression of the clinician performing the test. Although myometrial thickness at the various uterine regions cannot be easily assessed with endoscopic techniques, it can be measured with ultrasound or MRI.
2. Uterine wall thickness- This is the distance between the line connecting the tubal ostia and the external uterine profile obtained with 3D US, MRI and, at times, with 2D US

American Fertility Society has classified the malformations (Figure 10) as:

Figure 10 ASRM classification of Mϋllerian anomalies

Class I: Agenesis or Hypoplasia—
Segmental or Complete
Agenesis or hypoplasia may involve the vagina, cervix, fundus, tubes or any combination of these. Mayor-Rokitansky-Kuster-Hauser (MRKH) syndrome is the most well known example of this.

Class II: Unicornuate Uterus with or
without Rudimentary Horn
When an associated horn is present, this class is subdivided into communicating (continuity with main uterine cavity documented) or non-communicating. The noncommunicating variety is further subdivided on the basis of whether endometrium is present or absent in the rudimentary horn. The clinical significance of these types is that they are invariably associated with ipsilateral renal and ureteric agenesis.

Noncommunicating accessory horns that have endometrial cavity are the most common unicornuate subtype and are clinically important too. They are associated with high morbidity and mortality. When the accessory horn becomes obstructed, complication like hematometra can occur. There is also a risk of developing endometriosis.

Although normal pregnancies do occur, this type is associated with poorest obstetrical performance. This may be due to diminished uterine vasculature of deficient uterine musculature. A study12 of 393 pregnancies revealed 54.2 percent had normal deliveries, 43.3 percent had preterm deliveries, 4.3% had ectopic pregnancies and 34.4 percent had spontaneous abortions. About 2 percent pregnancies occur in accessory horn. Hence the noncommunicating horn should be excised prior to pregnancy.

  External contour Uterine cavity Separation of horns Cervix
Normal Convex, flat or, 1 cm fundal cleft Convex or flat (Two corneal ostia) Single triangular cavity Single
Unicornuate Convex or flat Convex or flat (single corneal ostium) Single banana shaped cavity Single
Didelphys Two well formed uterine cornu, convex or flat Two well formed uterine cornu with convex fundal contour in each with no communication Two horns widely divergent, at an obtuse angle Double
Bicornuate Fundal cleft >1cm Two well formed symmetric uterine cornu with convex fundal contour in each fused caudally, communicate Two horns widely divergent, at an obtuse angle Single or Double
Septate Convex, flat or <1 cm fundal cleft Two well formed symmetric uterine cornu, communicate Two horns close, acute angle at the center Single
Subseptate Convex, flat or <1 cm fundal cleft Two well formed symmetric uterine cornu, communicate Two horns close, acute angle at the center Single
Arcuate Convex, flat or <1 cm fundal cleft Single cavity with a broad shallow indentation Obtuse angle at the center Single

Class III: Didelphys Uterus
Complete or partial duplication of vagina, cervix and uterus is a feature of this type.

About 11 percent of all uterine abnormalities are of this type. Complete type is characterized by two hemiuteri, two endocervical canals, with cervices fused at the lower uterine segment. Each hemiuterus is associated with a fallopian tube. Ovarian malposition may also be present. The vagina may be single or double; more commonly double (75%). Occasionally, the vaginal septum may be transverse.

This type is associated with renal abnormalities in 20 percent of the cases. A syndrome called is Wunderlich-Herlyn-Werner syndrome has been described13. This consists of obstructed unilateral vagina with uterus Didelphys with ipsilateral ureteric and renal agenesis.

Class IV: Bicornuate Uterus—Complete or partial
Complete bicornuate uterus is characterized by a uterine septum that extends from the fundus to the cervical os. Partial type has a septum which is limited to the fundus. In both, there is a single cervix and vagina. Obstetric outcome depends on the length of the muscular septum, i.e. whether the bicornuate uterus is complete or partial. A partial bicornuate uterus has a 28 percent incidence of spontaneous abortion while in case of a complete bicornuate uterus; the incidence of abortion is 66 percent.

Class V: Septate Uterus—Complete or partial
A single uterus has a complete or partial septum. The septum is located in the midline fundal region. It is made up of poorly vascularized fibro muscular tissue. There are various variations of the septum. Sometimes a complete septate uterus is associated with a septate vagina. A variant septate abnormality exists which is characterized by the triad of complete septate uterus, duplicated cervix and septate vagina.14 It is undistinguishable from uterus Didelphys except by doing laparoscopy or a 3D USG. On laparoscopy, it is identified by its convex external contour.

A rare variant of septate uterus is Robert uterus.15 This is characterized by a complete septum and a noncommunicating hemiuteri with a blind horn.

Patients with a septate uterus have no difficulty in conceiving. Yet, they have poorest reproductive outcome of all the Müllerian anomalies.

Class VI: Arcuate Uterus
A small septate indentation is seen at the fundus.

Class VII: DES Related Abnormalities
A “T” shaped uterine cavity is seen.
Defects Not Classified by the AFS
• Transverse vaginal septum
• Vaginal Atresia

The ESHRE/ESGE classification
It was believed that the existing AFS classification had limitations (20). There was need to have a classification that was:
1. Clear and accurate
2. Which correlated with patient management

3. was simple and friendly

Müllerian Aplasia
This basically includes management of vaginal agenesis or MRKH syndrome. Here, the management comprises of two parts:
1. Creation of neovagina
2. Fertility treatment

Creation of Neovagina
Two methods have been described, nonsurgical and surgical. The nonsurgical method basically involves use of prosthetic moulds which deepen the existing pouch to create a satisfactory space for coitus. While surgical methods involve creation of neovagina, the strategy is to develop a space between the rectum and the bladder. Various tissues have been used to cover the newly created space. Full thickness or part thickness skin grafting is the most popular technique. However, skin grafting is associated with scar formation or contractures. Alternately, human amnion, not stripped from chorion is used as a graft material.16

More elaborate plastic surgical techniques include use of transposition flaps and autologous buccal mucosa. Use of artificial dermis and absorbable adhesion barrier shows promise as exogenous graft material to be used in neovagina. Interceed (Ethicon) has been used as an absorbable adhesion barrier. The neovagina epithelializes within 1 to 4 months.
Some surgeons use a bowel segment in place of skin graft. However, this is associated with troublesome leucorrhea after the surgery.

Fertility Treatment
Since, most of these women have healthy and functioning ovaries; surrogate pregnancy is a viable treatment modality.

Unicornuate Uterus
The indication for surgery is presence of endometrium in the rudimentary horn. In case the rudimentary horn does not have a functioning endometrium, then surgical intervention is not indicated.

In case surgery is contemplated, laparoscopic hemihysterectomy of the rudimentary horn is the procedure of choice. The rudimentary horn is connected to the functioning unicornuate uterus by a fibromuscular band. This band is of importance as the uterine artery courses inferior to it. The pedicle of the rudimentary horn is coagulated using bipolar cautery. Tube and the rudimentary horn are removed, leaving ipsilateral ovary which is usually healthy, in situ.

In the event of pregnancy in the rudimentary horn, same procedure as nonpregnant uterus is followed. However, there is a risk of increased bleeding due to pregnancy related vascularization. Methotrexate has been used to treat the pregnancy before surgical removal of the rudimentary horn.

Hysteroscopic endometrial ablation of the rudimentary horn has been reported.17

Uterus Didelphys
Guidelines for surgical intervention are as follows:
1. Uterus didelphys with obstructive vaginal septum—Full excision and marsupialization of the vaginal septum is the treatment of choice. After the septum is excised, laparoscopy may be indicated as these cases are associated with endometriosis.
2. Uterus didelphys with nonobstructive vaginal septum—surgery is indicated if the patient complains of dyspareunia.
3. Currently, metroplasty is not indicated in cases of nonobstructive didelphys uterus.

Bicornuate Uterus
Guidelines for surgical correction are as follows:
1. Bicornuate uterus seldom requires surgical management.18
2. Metroplasty should be reserved for those women with repeated pregnancy losses or rarely in those in whom no other cause for infertility is detected.

Septate Uterus
Uterine septum is associated with primary infertility, recurrent miscarriages and preterm labor. In such cases, hysteroscopic resection of the septum is indicated.19 The decision to operate should be taken only for poor reproductive performance.

ESHRE/ESGE consensus on workup of female genital anomalies (21)

Recommended evaluation of asymptomatic women
Clinicians should, always, be attentive for the presence of a congenital anomaly in asymptomatic women of reproductive age during their routine examination, supplementing gynaecological examination with a 2D US as follows:
Gynecological examination: the anatomy of the external genitalia, the vagina and the cervix should be carefully evaluated.
2D US: it should be done in a pre-defined and systematic manner to increase its diagnostic accuracy. The shape and the dimensions of the uterine cavity, the uterine wall (anterior, posterior, lateral and fundal width) and external uterine contour should be recorded in a systematic way in longitudinal and transverse planes.

The absence of findings suspicious for the presence of an anomaly should not be considered as definite and the presence of one could not be excluded.

Positive findings should be used for documentation only and counselling of the patients for further investigation given that they are asymptomatic women.

Recommended evaluation of symptomatic women
Gynecological examination with careful evaluation and recording of the external genitalia, vaginal and cervical anatomy.

2D US (vaginal) in a pre-defined and systematic manner (to increase its diagnostic accuracy), where the shape and the dimensions of the uterine cavity, the uterine wall (anterior, posterior, lateral and fundal width) and external uterine contour should be recorded in a systematic way and pre-defined way in longitudinal and transverse planes. Measurements of 2D US examination should be used as a referendum for the evaluation of uterine anatomy deviations in 3D ultrasound.

3D US (vaginal) in a pre-defined and systematic manner where the shape and the deviations from normal cervical and uterine anatomy should be recorded and documented.

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