1 Department of Obstetrics and Gynecology and 2 Department of Radiology, Ziekenhuizen Oost-Limburg, Schiepse Bos 6, 3600 Genk and 3 Department of Obstetrics and Gynecology, St Franciscusziekenhuis, P. Perquaylaan 129, 3350 Heusden-Zolder, Belgium
4 To whom correspondence should be addressed. e-mail: willem.ombelet{at}pandora.be
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Abstract |
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Key words: ectopic ovary/infertility/MRI/undescended ovary/unicornuate uterus
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Introduction |
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The incidence of congenital uterine malformations varies between 0.15.0% and Müllerian anomalies are found more often in subfertile patients compared with fertile and sterile controls (Acién, 1997; Raga et al., 1997
; Grimbizis et al., 2001
). Of all Müllerian defects, unicornuate uterus is found in 313% of cases (Acién, 1997
; Raga et al., 1997
; Grimbizis et al., 2001
). Unicornuate uterus is caused by a failure of one Müllerian duct to develop (unicornuate uterus without rudimentary horn) or to migrate to its proper location. It is linked to an increase in obstetrical complications such as early miscarriages, ectopic pregnancy, abnormal fetal presentation, intrauterine growth retardation and premature labour (Andrews and Jones, 1982
; Heinonen et al., 1982
; Donderwinkel et al., 1992
; Moutos et al., 1992
;; Heinonen, 1997
; Raga et al., 1997
). Despite the well-known association of ectopic ovaries and unicornuate uterus, ectopic ovaries are reported only sporadically, suggesting the possibility that many cases go unrecognized (Verkauf and Bernhisel, 1996
).
This is the first report on the use of magnetic resonance imaging (MRI) after ovarian stimulation in the detection of undescended ovaries. We describe four cases of unicornuate uterus in which the diagnosis of ectopic ovary during a routine infertility exploration including hysterosalpingography (HSG), hysteroscopy and laparocopy was missed.
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MRI techniques and methods |
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Case 1
A couple with primary infertility for 3 years was referred to our infertility centre for donor-insemination. Investigation of the male partner revealed azoospermia. Genetic testing proved to be normal. On testicular biopsy the diagnosis of Sertoli-cell only syndrome was made. An infertility work-up of the female, including an endocrinological and immunological evaluation, was normal. An HSG showed an unicornuate uterus with one patent salpinx on the right side (Figure1a) and this was confirmed laparoscopically. A urological examination including i.v. pyelography (IVP) could not detect any abnormality.
The couple was entered in our donor-insemination programme. Clomiphene citrate (CC) (50 mg for 5 days, days 59) for mild ovarian stimulation was used. In the first treatment cycle, we observed a normal bifollicular response with a serum estradiol level of 544 pg/ml on the day of hCG administration. This attempt was unsuccessful. In a consecutive cycle, serum estradiol reached a level of >600 pg/ml, but no ovarian response could be seen on ultrasound. A spontaneous LH surge was noted. In this cycle, we performed no insemination. Because an ectopic ovary was suspected, vaginal and abdominal ultrasound was carried out but could not confirm the diagnosis of an undescended ovary. During the next cycle and following CC stimulation, an MRI examination (Siemens I.O.T. magneton) was carried out on day 12 of the cycle. This confirmed the presence of a unicornuate uterus and revealed a left-sided undescended ovary at the level of the pelvic brim, anterior to the psoas muscle, containing several follicles (Figure 1bd). A thin cord-like structure continued from this ovary in the direction of the internal inguinal canal. The latter contained a small (15 mm diameter) nodular structure at the level of the external iliac vascular axis. This was considered to be a Müllerian remnant or a remnant of the lower gonadal cord. Considering these findings, the diagnosis of an ectopic ovary was made. The right ovary was entirely normal.
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The couple was advised to start with intrauterine insemination (IUI) after CC ovarian stimulation. On day 15 of the first IUI cycle, serum estradiol reached 272 pg/ml with only one follicle of 12 mm diameter visible on vaginal ultrasound. Because of the discrepancy between follicular size and estradiol level an MRI was performed confirming the presence of a left-sided ectopic ovary in the upper part of the pelvis, anterior to the intersection of the psoas and the iliac muscle. It contained numerous follicles (Figure 2).
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A male factor was found with unexplained oligoasthenoteratozoospermia. After the washing procedure, >1x106 motile spermatozoa could be recovered and therefore IUI treatment with CC ovarian hyperstimulation was continued (Ombelet et al., 1997b). During the next IUI treatment cycle a discrepancy between serum estradiol levels and ovarian ultrasound images (follicular growth) was observed. An ectopic ovary was suspected and MRI was carried out after mild ovarian CC stimulation. This confirmed the presence of a unicornuate uterus and a normal right-sided ovary containing numerous follicles. A left retroperitoneal ectopic ovary was seen as a cord-like structure that contained several follicles. Its cranial border reached the left side of the second lumbar vertebra, the caudal part of the cord-like ovary stretched to the internal inguinal canal (Figure 3). The left kidney was absent.
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Considering our experience with the previous cases of unicornuate uterus, MRI after CC ovarian stimulation was performed. During that cycle one dominant follicle was observed with a diameter of 16 mm in the left ovary. Serum estradiol levels reached 610 pg/ml, again showing a discrepancy between ultrasound findings and serum hormonal level. MRI confirmed the presence of an undescended ovary at the right pelvic brim, anterior to the psoas muscle, containing several follicles (Figure 4).
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Cases 58
The next four patients were found to have a unicornuate uterus on routine fertility exploration in our centre. Because of the previous experience, MRI after CC stimulation was conducted in all cases resulting in one extra case of undescended ovary. In this patient, the undescended ovary could also be visualized on abdominal ultrasound. In three other patients, two normally localized ovaries were observed without the presence of an ectopic ovary. In two patients a rudimentary horn was diagnosed on MRI.
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Discussion |
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The embryological mechanism underlying undescended ovaries is uncertain, but could be explained by a lack of caudal descent of the gonads into the true pelvis (Parmley, 1993) or by a retarded differential growth of that portion of the urogenital ridge giving rise to both the gonad and the Fallopian tube (Rock et al., 1986
). Ectopic ovaries may be unilateral or bilateral and can be associated with abnormalities of the Müllerian ducts such as unicornuate uterus. The association of unicornuate uterus and urinary tract anomalies including ectopic kidney, renal agenesis, double renal pelvis and horseshoe kidneys is well known (Fedele et al., 1996
).
In this study we describe four cases of true embryologic undescended ovaries, with attachment of the upper pole to an area above the level of the common iliac vessels. All four cases were missed by routine fertility exploration. In three cases (reports 1, 2 and 3) MRI was performed after mild ovarian stimulation with CC because a discrepancy between serum estradiol levels and ovarian ultrasound images was found after ovulation induction. The multifollicular growth in the ectopic ovary greatly enhanced MRI diagnosis.
State-of-the-art MRI has proven its value in the detection and characterization of a wide variety of disorders of the female reproductive organs. Ultra-fast cross-sectional T1- and T2-weighted images can be used to assess the normal and pathological ovaries. Usually, MRI is used as an adjunct to ultrasound and/or computed tomography in selected cases. However, while reports documenting the value of MRI in detecting anomalies of the uterus and ovaries are profound in the literature, reports concerning the detection of ectopic ovaries are lacking.
As described in these case reports, we used MRI as the primary imaging tool to detect the location and the appearance of the contralateral ovary in those patients with an unicornuate uterus. MRI was chosen because this technique has a superior soft tissue contrast, has multiplanar imaging capabilities and lacks ionising radiation. MRI was shown to be more sensitive in the detection of an undescended ovary compared with ultrasound.
A review of the literature revealed one case of a supernumerary ovary in a patient with persistent elevated plasma estrogen levels despite bilateral oophorectomy. The ectopic ovary in that particular patient was diagnosed by stimulation with hCG (Kosasa et al., 1976).
Although the incidence of unicornuate uterus is low, a correct diagnosis is mandatory not only to be aware of the existence of an ectopic ovary but also in considering the reproductive performance when uterine malformations are involved. Early and late abortions as well as preterm delivery are found much more often if unicornuate uterus is involved (Andrews and Jones, 1982; Donderwinkel et al., 1992
; Moutos et al., 1992
; Heinonen, 1997
; Raga et al., 1997
). Concerning assisted reproduction, significantly lower implantation rates are described after IVFembryo transfer in cases of unicornuate uterus (Heinonen et al., 2000
).
The knowledge of the existence of an ectopic ovary is also of importance and relevant in the following clinical situations: follicle aspiration techniques in women with unicornuate uterus, exploration of unexplained cyclic abdominal pain due to folliculogenesis, ovulation and cyst formation in the undescended ovary and medical conditions where surgical castration is indicated.
There are many reasons to promote MRI after mild ovarian stimulation in all cases of unicornuate uterus. Stimulation with CC improves the accuracy of the MRI examination. Therefore we suggest performing routine MRI after CC stimulation in all unicornuate uterus cases. Whether MRI in a non-stimulated cycle is as sensitive as MRI after CC stimulation is doubtful, but has to be investigated.
Continuous refinement of the MRI technique and further improvement of the spatial resolution and increased availability of MRI will progressively increase its application in the detection of undescended ovaries and other Müllerian fusion defects. Since both intra- and extra-peritoneal locations of an undescended ovary may occur, the authors suggest that MRI can precede or replace laparoscopic evaluation in this specific patient population (Doyle, 1992).
There are enough reasons to prefer MRI above laparoscopy in the diagnosis of undescended ovaries: (i) the costs (for society) of a laparoscopy are much higher compared with MRI; (ii) in contrast with laparoscopy, MRI is a non-invasive procedure; and (iii) renal abnormalities and extra-peritoneal ovaries (which are probably the most important to diagnose) cannot be evaluated during laparoscopy.
To conclude, MRI after CC ovarian stimulation in all unicornuate uterus cases may avoid otherwise invasive diagnostic techniques and could detect undescended ovaries more frequently than has been appreciated to date. We described a novel and sensitive tool in the diagnosis of undescended ovaries, an entity which has probably gone unrecognized until now in many patients at risk.
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Acknowledgements |
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References |
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Submitted on August 19, 2002; resubmitted on November 6, 2002; accepted on January 9, 2003.