Intrauterine adhesions combined with Robert’s uterus: a case report and literature review

To summarize the clinical characteristics and surgical option of Robert’s uterus. We reported a rare case of Robert’s uterus with severe uterine adhesion with successive laparoscopic and hysteroscopic surgery. To our knowledge, such a case has not been reported previously. We also performed a systematic literature review from the PubMed, Embase, and Cochrane databases. Our patient with Robert’s uterus with severe uterine adhesions was successfully treated with hysteroscopic septal resection and hysteroscopic adhesiolysis, and the intractable dysmenorrhea disappeared after the hysteroscopic septal resection. In our study, we analyzed the selected 22 reported cases, 10/22 cases (45.5%) were diagnosed before age 20; 20/22 cases (90.91%) experienced dysmenorrhea, 19/22 cases (86.36%) were with hematometra. 5/22 cases (22.73%) underwent re-operation or a third surgery before diagnosis and management. Robert's uterus, a rare congenital abnormality of Mullerian duct development, consists of an oblique septum and non-communicating asymmetrical uterine hemi-cavity. The main symptoms are the presence of hematometra and severe dysmenorrhea. Septal resection is the main surgical procedure; however, the rarity and difficulty obtaining a pre-operative diagnosis lead to a high rate of misdiagnosis and second surgery.


Introduction
Robert's uterus is a rare Mullerian abnormality characterized by an asymmetrical septum, first reported by Robert in 1970. To date, more than 20 cases of Robert's uterus have been reported. Robert's uterus is a rare congenital abnormality consisting of a uterine septum asymmetrically separating the uterine cavity from the bottom of the uterus, half of which is a disconnected blind cavity [1]. Gupta et al. suggested that a blind cavity commonly develops on the right side, because the left Mullerian duct develops first, embryologically [2]; however, a blind cavity was more commonly left-sided, in the review. Musset et al. [3] summarized the characteristics of Robert's uterus as: (1) primary dysmenorrhea; (2) no significant difference in the uterus laparoscopically, and a unicorn uterine cavity found on hysterography; and (3) no deformity of the urinary system. Most patients complain of dysmenorrhea, periodic abdominal pain, abnormal menstruation, miscarriage, or infertility. Ultrasonography, magnetic resonance imaging (MRI), hysteroscopy, and laparoscopy have been performed to diagnose Robert's uterus. No standard surgical options are recommended recently and different operative approaches on Robert' uterus have been reported. However, diagnosing Robert's uterus remains a challenge, especially regarding differentiating serious dysmenorrhea from other acute abdominal diseases, some authors have reported re-operation or a third surgery before diagnosis and management.
In concordance with these findings, the current patient underwent surgical treatment twice and was also complicated with severe intrauterine adhesions, which has not been mentioned in the previous literature. Hence, we also performed a systematic literature review to improve pre-operative diagnosis and to avoid inappropriate operation. The literature search was performed in PubMed, Embase, and Cochrane library from inception to March 2021. We used a combination of free terms and MeSH terms as search strategies: the MeSH terms "uterus" and the subheading "abnormalities", combining the free terms of "Roberts uterus" or "genital tract abnormalit*" or "Mullerian abnormality*" or "septate". As shown in the flowchart (Fig. 1), a total of 1410 records were identified using search strategies. Literature with complete clinical features published in English language was included; the forms of brief description or video presentation, as well as other irrelevant literature were excluded. Finally, 18 full-text articles meeting the inclusion criteria were included in the literature review.

Case presentation
A 24-year-old married woman suffered reduced menstruation and lower abdominal pain associated with her menstrual period since the age of 22 years, especially before and on the first day of menstruation. The frequency of pain increased afterward (from once every 3 months to once a month) and progressed (from spontaneous remission without the assistance of medications to pain requiring drug assistance). Two months before presenting to our institution, the patient presented to the emergency department of a local hospital owing to severe abdominal pain accompanied by nausea and vomiting. Ultrasonography revealed intrauterine fluid measuring 13 × 20 × 10 mm, and a cystic mass in the right parametrium space measuring 32 × 23 × 20 mm. There was also an isoechoic and hyperechoic cyst on the right ovary measuring 55 × 60 × 57 mm. Emergency laparoscopic surgery was performed for the suspicion of ovarian teratoma torsion, which revealed severe pelvic adhesions, normal uterine size, right hematosalpinx, as well as a cystic mass on the right ovary, without torsion. Laparoscopic right ovarian cystectomy, right salpingectomy, and pelvic adhesiolysis were performed. The pathological diagnosis was ovarian mature cystic teratoma and right fallopian tube endometriosis. However, the patient presented to our center for unrelieved abdominal pain postoperatively. At the second presentation, the left endometrial thickness was 4 mm, and right uterine cavity fluid measured 42 × 19 mm. The size of the anechoic area in the right uterine horn was 23 × 15 mm, and the area appeared to communicate with the right uterine cavity (Fig. 2a). Three-dimensional ultrasonography (3D-US) confirmed the presence of an oblique septum and fluid in the blind uterine cavity (Fig. 2b). MRI showed a septum in the uterus dividing the endometrial cavity into two cavities of unequal size (Fig. 3a), with hematometra within the right uterine cavity, which was disconnected form the other cavity connecting to the cervix (Fig. 3b); and  Fig. 2 a Ultrasonography revealed an anechoic zone of hematometra in the right uterine cavity (+). b Three-dimensional ultrasonographic image showed a uterine malformation appearing as the presence of an oblique septum (*) and hematometra (+) in the blind uterine cavity hematometra, mainly in the right smaller cavity, mimicking a unicornuate uterus with a communicating rudimentary horn (Fig. 3c). Physical examination and laboratory blood examination findings were normal. Ultrasoundguided hysteroscopic surgery was performed, which revealed a small narrow uterine cavity with one horn communicating with the cervical canal and biased to the left side. The fundus and left wall of the uterine cavity had severe adhesions with a thin endometrium, and the left fallopian ostium was invisible. A fibrous oblique diaphragm was present on the right side of the uterine cavity, with a slight bulge. The right uterine cornu and fallopian ostium were invisible (Fig. 4a). After gently separating the weakest part of the diaphragm along the bulge using a needle electrode, dark-brown hematocele liquid spilled out, and the oblique septal tissue was gradually removed using band electrodes along the opening. Then, the right-side uterine cavity and the right cornu were exposed, and we separated the intrauterine adhesions with needle electrodes to recover normal uterine morphology. A Foley catheter inflated with 3 ml of saline was placed in the uterine cavity for 7 days to prevent intrauterine adhesion recurrence. The patient was discharged 2 days after the operation. Estrogen and progesterone sequential treatment was prescribed to prevent recurrence. Four weeks after the operation, repeat hysteroscopy showed a normal-appearing cavity and endometrium (Fig. 4b). The intractable dysmenorrhea of the patient was disappeared gradually at follow-up for 2 years after the operation. Fig. 3 a MRI showed that a septum in the uterus divided the endometrial cavity into two cavities (+) (*). b Hematometra within the right uterine cavity was disconnected form the other cavity connecting to the cervix (+) (*). c MRI revealed that hematometra within the right uterine cavity appeared to communicate with the smaller cavity in the right uterine cornu (#)

Discussion
Robert's uterus is characterized by a non-communicating intrauterine cavity and unilateral hematometra in a blind uterine cavity owing to the oblique septum. Progressively significant dysmenorrhea or severe abdominal pain are the main symptoms [1][2][3]. Intractable dysmenorrhea appears to be associated with concurrent hematometra. With hormonal stimulation, menstrual blood induced by endometrial shedding could flow retrograde into the abdominal cavity through the ipsilateral fallopian tube during menstruation; thus, initially, dysmenorrhea in Robert's uterus is periodic and not obvious. Then, with the ipsilateral fallopian tube gradually thickened, the tube becomes blocked, and blood accumulates. As a result, dysmenorrhea gradually worsens owing to the formation of a closed cavity, which may be associated with inflammation or endometriosis. We identified 22 cases in our systematic literature review (  [4,6,8,18], and 2/22 cases (9.09%) experienced infertility [14]. 10/22 cases (45.5%) were diagnosed before age 20. 8/22 cases (36.36%) of endometriosis have been documented in patients performed laparoscopy or laparotomy [3-6, 8, 11, 15]. Gupta et al. proposed that endometriosis may be associated with menstrual blood reflux in Robert's uterus [3]. In our case, after resecting the right fallopian tube, the blind cavity was visibly completely disconnected from outside the uterus. As a result, increased pressure was associated with the retention of menstrual blood in the closed right-sided uterine cavity, which induced worsened abdominal pain.
Ultrasonography, MRI, hysteroscopy, and laparoscopy have been performed to diagnose the Robert's uterus. The septum, with asymmetrical uterine cavities, is easily discernible, and hematometra and hematosalpinx are easy to identify with noninvasive imaging modalities, such as 3D-US and MRI, which are considered reliable modalities to examine uterine morphology [14,19]. Even 3D-US are considered better than MRI in diagnosis of Robert's uterus for its frugality and easy availability [4]. In the literature,  [20]. In addition, we strongly recommend a detailed inspection of the urinary system in similar cases, considering that two cases of ipsilateral renal agenesis have been reported [7,8]. To the best of our knowledge, our patient is the first case of Robert's uterus in combination with intrauterine adhesions, which was verified by hysteroscopy. Our patient had no history of intrauterine operation, such as induced abortion, which may be related to obstruction of menstrual blood outflow and inflammation, and there was no evidence of endometritis. In our opinion, early diagnosis and hysteroscopic surgery may reduce the incidence of these complications. However, the early diagnosis of uterine malformation by ultrasonography or MRI is significantly affected by the examiner's skill level. Successful management depends on accurate pre-operative diagnosis. In the literature, 5/22 cases (22.73%) underwent re-operation or a third surgery before diagnosis and management [3,4,6,7,12]. Some of the Robert's uterus have normal external uterine contour [12], making it difficult to identify by laparoscopic surgery. We recommend that if the intraoperative findings are inconsistent with the clinical manifestation of severe abdominal pain, uterine inspection via hysteroscopy is needed. Patient trauma can be reduced with adequate evaluation and determining the pre-operative diagnosis.
Surgical treatment is the only recommendation and surgical options should be determined by the patient's age and fertility desires. The primary surgical goals are draining the hematometra and preventing its recurrence through septal resection [11]. Laparoscopic septal resection and metroplasty are considered, for the minimal invasiveness, especially for adolescent girls. 21 of the 22 Robert's uterus underwent surgery (Table 2). In 13/21 cases, septal resection was performed by laparoscopy, hysteroscopy, or laparotomy [1, 3-5, 7-10, 12-16]. One case underwent hysterectomy due to lack of fertility requirement [4]. Hysteroscopic septal resection and laparoscopy guidance are the main option for the surgical treatment with the minimal invasive [1,8,10,14], laparoscopy could identify the hematosalpinx, pelvic adhesions, and endometriosis, which cannot be evaluated by auxiliary examination, and, remarkably, hysteroscopic surgery performed by experienced surgeons is essential for the complicated environment in uterus; It has been reported that a patient whose Robert's uterus underwent hysteroscopic treatment combined with the laparoscopic instrument was successfully pregnant and gave birth [15]. Summary of the statistical characteristics is from the literature review (Table 3). If our patient has fertility requirements in the future, salpingography can be done first to determine whether the left fallopian tube is unobstructed, and then decide about the  [6] Right Hysterectomy and right salpingectomy Two Liu Y. 2020 [7] Right Hysteroscopic septal resection and laparoscopic right salpingectomy Two Yang QM. 2019 [8] Right Hysteroscopic septal resection and laparoscopy guidance One Shah N. 2019 [1] Left Hysteroscopic septal resection and laparoscopy guidance One Kiyak H. 2018 [9] Right Laparoscopic septal resection One Biler A. 2017 [10] Right Hysteroscopic septal resection and laparoscopy guidance One Mittal P. 2017 [11] Left Laparotomy excision of the blind cavity One John SK. 2017 [12] Right Laparotomy septal resection Three Ludwin A. 2016 [13] Left Hysteroscopic septal resection One Di Spiezio SA. 2015 [14] Left Hysteroscopic septal resection and Laparoscopy guidance One Li J. 2015 [15] Left Laparotomy septal resection and laparoscopic oophorocystectomy One Maddukuri SB. 2014 [16] Left Laparotomy septal resection One Vural M. 2011 [17] Left Laparotomy endometrectomy of the blind cavity One Capito C. 2009 [2] -Laparotomy endometrectomy of the blind cavity One Gupta N. 2007 [3] Right Laparotomy septal resection Two Singhal S. 2002 [18] Right Laparotomy One 1 3 need of assisted reproduction. Monitoring the situation of pregnancy and appropriate intervention to achieve better pregnancy outcomes if required.
In conclusion, Robert's uterus is a congenital abnormality that has an oblique septum and non-communicating asymmetrical uterine hemi-cavity, and the case report and literature review providing detailed clinical features contribute to improving the diagnosis and treatment. Despite the strengths, diagnosing preoperatively remains a challenge for its rarity and the high risk of misdiagnosis, and thus, more studies need to be investigated.