Acién, Pedro MD, PhD, FRCOG; Acién, Maribel MD, PhD; Fernández, Fátima MD; José Mayol, María MD, PhD; Aranda, Ignacio MD, PhD
Potter and Schenken1 described the case of a 15-year-old girl with a noncommunicating accessory uterine cavity and normal uterus. It was then considered a rare Müllerian anomaly, not included in the usual classification systems and difficult to explain by embryology. Other similar cases have been published as juvenile or isolated cystic adenomyomas,2–5 sometimes considered as a condition not previously reported in the literature. These supposed juvenile and isolated cystic adenomyomas are different from true adenomyomas with an internal cystic area or degeneration associated with adenomyosis, leiomyomas, or both observed in older women.
We suggest the hypothesis that most published cases of juvenile cystic adenomyomas, as well as those cases of noncommunicating accessory uterine cavities and some cases of uterine-like masses, are actually the same pathology: an accessory and cavitated uterine mass with functional endometrium representing a new type of Müllerian anomaly. This has important clinical manifestations and is problematic because of the broad differential diagnosis, which includes the rudimentary and cavitated uterine horns found in other uterine malformations (bicornuate uterus and segmentary atresias) and the ademomyomas with cystic or degenerated areas.
The objectives of this article are as follows: 1) to review the literature and present clinical cases of women who had an accessory noncommunicating uterine cavity with functioning endometrium associated with a normal uterus, similar to other cases already published as juvenile or isolated cystic adenomyomas; 2) to show that both accessory uterine cavities and isolated cystic adenomyomas represent the same pathology and that they are different from other cases of true adenomyomas that can have an internal cystic or degenerated area; and 3) to suggest that the accessory and cavitated uterine mass actually represents a new type or variety of Müllerian anomaly, generally located at the level of the insertion of the round ligament, possibly related to a dysfunction of the female gubernaculum and always observed in women with an otherwise normal uterus.
MATERIALS AND METHODS
A review of the literature was performed through a MEDLINE search by looking for “accessory uterine cavity,” “cystic adenomyoma,” “cystic adenomyosis,” “adenomyotic cyst,” “uterine adenomyomas,” “uterus-like mass,” “Müullerian anomalies,” “non-communicating uterine horn,” and “cavitated rudimentary uterine horn.” Table 1 lists cases that are described as accessory uterine cavities, as juvenile or isolated cystic adenomyomas, or as uterine-like masses that we think could be an accessory and cavitated uterine mass (accessory uterine-like). The criteria used to include a case as accessory and cavitated uterine mass were: 1) an isolated accessory cavitated mass; 2) normal uterus (endometrial cavity), tubes, and ovaries; 3) surgical case with excised mass and with pathological examination; 4) accessory cavity lined by endometrial epithelium with glands and stroma; 5) chocolate-brown–colored fluid content; and 6) no adenomyosis (if uterus removed), but there could be small foci of adenomyosis in the myometrium adjacent to the accessory cavity.
Apart from the four cases presented in this article, 14 cases have been found in the literature with the described characteristics, but another 11 published cases are doubtful and are included in Table 2. Other reviewed cases21–24 were found to be cystic adenomyosis or they corresponded to rudimentary and cavitated uterine horns (bicornuate uterus) or to uterus didelphys with unilateral cervicovaginal atresia and ipsilateral renal agenesis.25–27 Therefore, they have not been included.
We present here four cases of a noncommunicating accessory uterine mass in individuals whose genital tracts were well-studied with hysterosalpingogram, ultrasound imaging, and postoperative pathology. These four women did not have a typical uterine malformation, but they presented with prominent symptoms and an intramural or subserous mass located in the anterior uterine wall at the level of the insertion of the round ligament (three on the right, one on the left). We performed excision of the tumor in three women and hysterectomy in one woman, all of them with histopathological study.
Likewise, although we reviewed several other cases of adenomyomas, for the purpose of aiding differential diagnosis, we also present here another case of a cavitated adenomyoma (case 5) that underwent surgery because of pain, metrorrhagia, and uterine tumors that corresponded to a true adenomyoma with adenomyosis and leiomyomas.
Written informed consent was obtained from each individual for the study, surgery, and scientific publication. Ethical approval was granted by Comité Ético de Investigación Clinica, San Juan University Hospital (but this is not required for case studies in Spain).
A 15-year-old girl presented at the emergency department because of severe, right hypogastric pain recurrent for more than 1 year. The pain persisted for 2 to 3 days, every second month. Her periods were regular, occurring every 30 days. The speculum examination was normal and bimanual examination suggested a leiomyoma on the right uterine horn. Transvaginal ultrasonography showed a normal uterus and an intramural or subserous leiomyomalike mass. The mass was cavitated and appeared to be a rudimentary uterine horn with an endometrial cavity containing thick endometrium (Fig. 1A). The ovaries were normal. Complete blood counts and intravenous pyelography were normal, and hysterosalpingogram showed a normal endometrial cavity with patent fallopian tubes (Fig. 1B). We performed a laparotomy and found a mass on the right anterior uterine wall at the level of the right round ligament insertion that appeared similar to a leiomyoma (Fig. 1C, D). During tumor excision, chocolate-brown–colored blood leaked from a partial break in the mass. There was no communication with the main endometrial cavity. The rest of the genital tract was normal. Histopathology of the excised lesion confirmed the presence of a myometrial wall with an atrophic internal endometrial lining. This young individual's follow-up has been normal; dysmenorrhea and abdominal cramps completely disappeared postoperatively.
A 21-year-old woman with a previous cystectomy of a right ovarian endometrioma performed at another hospital 2 years before presented at our center and was referred for severe dysmenorrhea and hypogastric pain for the past 3 years. The examination, including a transvaginal ultrasound examination, revealed a 3-cm cavitated mass on the left uterine horn, suggestive of a cavitated adenomyoma (Fig. 2A). Complete blood count and tumor markers were normal, and hysterosalpingogram showed a normal uterus with patent tubes. During laparotomy, we observed dense adhesions at the pouch of Douglas and a tumor at the insertion of the left round ligament. Excision was difficult because of ill-defined borders and significant vascularization. Histopathology revealed a cavitated adenomyomalike mass with an internal endometrial lining (Fig. 2B, C). Follow-up has been normal, with asymptomatic menstruations, for 18 months after surgery.
A 33-year-old woman without previous pregnancies presented with daily right iliac fossa pain during the previous few months. Ultrasound examination showed a 3-cm cavitated mass with endometriomalike contents, contiguous with the right uterine horn (Fig. 3A). Hysterosalpingogram showed a normal uterus with patent tubes (Fig. 3B). She underwent laparoscopy that revealed a subserous myomalike formation under the right round ligament insertion. We performed a tumor excision, and the histopathological study showed a cavitated adenomyomalike mass with an internal endometrial lining (Fig. 3C). This individual has been asymptomatic on subsequent follow-ups.
A 32-year-old woman with a previous normal delivery and three cesarean deliveries was referred to the outpatient clinic with intense dysmenorrhea, dyspareunia, right iliac fossa pain, and hypermenorrhea. The pelvic examination was painless but revealed a right anterior uterine formation. Ultrasonography demonstrated a 5-cm cystic tumor with endometriomalike characteristics and thick walls, independent from the right ovary. Complete blood count and tumor markers were normal. Surgery was complicated by multiple adhesions from previous surgeries and revealed a soft myomalike tumor on the right anterior uterine wall, a right hydrosalphynx, and a right paraovarian cyst. A total simple hysterectomy with right salpingectomy and paraovarian cyst excision was performed. A section of the tumor spilled abundant chocolate-brown–colored fluid (Fig. 4A), but the uterine endometrial cavity was normal. Pathology revealed the presence of a 5-cm cystic adenomyomalike mass on the right anterior uterine wall with an endometrioid lining of the cystic cavity (Fig. 4B, C), in addition to a right hydrosalphynx and a right Müllerian cyst. This individual has been asymptomatic for 12 months after surgery.
A 48-year-old woman presented with severe pain and hypermenorrhea. Pelvic examination and transvaginal ultrasonography revealed multiple leiomyomas, some of which were submucosal, and a cavitated adenomyoma (Fig. 5A). She had a history of primary infertility and was evaluated with a hysterosalpingogram, which showed a normal uterus with patent tubes (Fig. 5B). Treatment with in vitro fertilization resulted in two pregnancies delivered by cesarean. More recently, she had been administered GnRH analogs with add-back therapy because of poor tolerance of menopausal symptoms. We performed a simple total hysterectomy without complications. Macroscopic and microscopic studies of the surgical specimen showed leiomyomas, multiple foci of adenomyosis in the uterine wall, and a cavitated adenomyoma with internal proliferative adenosis (Fig. 5C). Histopathological study of the cavitated adenomyoma showed an absence of an internal endometrial lining but severe adenomyosis in the wall (Fig. 5D, E).
As shown in Table 1, there are 18 reported cases (including the four cases reported in this article) that match the inclusion criteria listed for accessory and cavitated uterine mass associated with an otherwise normal uterus. In addition, another 11 cases only partially fulfilled the inclusion criteria and are included in Table 2. The average age of women with the cases was 24 years (range 15–36 years). They were published as cases of cystic adenomyoma or an accessory uterine-like mass located in the anterior surface of the uterus in the attachment area of the round ligament (six on the left, eight on the right, three unstated).10 All cases presented as similar, serious clinical manifestations. In each case, histopathology revealed a cystic adenomalike mass with an internal cavity lined with endometrium and an external muscular wall.
Excluding the case reported by Fisseha et al (in a 13-year-old, without surgery), notably, the average age of women with the 10 remaining doubtful cases was 43 years (range 26–57 years). They were published as congenital or adenomyotic cysts of the uterus or as uterine-like masses located in various sites in the pelvis, attached or not to the uterus. Ahmed et al15 presented a case of a uterine-like mass as a rudimentary horn with a third fallopian tube and the characteristics of a duplication of the right Müllerian duct, which is different from the accessory uterine masses.
Our first four cases were found in young women presenting with an anterior uterine mass who were referred for severe dysmenorrhea and abdominal cramps. On transvaginal ultrasonography, the tumors looked like an accessory and cavitated uterine horn. However, the uterine shape was shown to be normal at hysterosalpingogram and surgery. In all of these cases, the tumor was intramural and subserous and located in the anterior wall of the uterus at the level of insertion of the round ligament. In case four, we also found a paraovarian cyst with paramesonephric epithelium on the same side as the tumor. As noted, Figures 4B and 4C show the histopathology of the huge right accessory and cavitated uterine mass observed in this case, with a myometrial wall lined internally by endometrioid epithelium with some glands in the stroma.
Individuals with true adenomyomas are older women presenting with adenomyosis and adenomyomas, some with internal cystic areas, and frequently associated with leiomyomas. This is illustrated by our case five. Case five also had severe pain and hypermenorrhea. This was a true adenomyoma with a cystic area with adenosis confirmed by histopathology showing multiple foci of adenomyosis within the smooth muscle bands and an absence of an internal epithelial lining (Fig. 5C, D). This is distinct from what is shown in Figures 4B and 4C, corresponding to the huge cavitated accessory uterine mass.
As shown in our four cases and analysis of other published cases, noncommunicating accessory uterine cavities and isolated or juvenile cystic adenomyomas actually have the same pathology and can be defined as accessory and cavitated uterine mass without malformation of the eutopic uterine endometrial cavity. They present in young women; have important clinical manifestations of pelvic pain, severe dysmenorrhea, and abdominal cramps resistant to drug therapy; and are clearly different from true cavitated adenomyomas in terms of clinical presentation, ultrasonography, surgical findings and histopathology. These adenomyomas frequently are associated with leiomyomas, cause hypermenorrhea in perimenopausal women, and have adenomyosis and an absence of an internal epithelial lining on histopathology. Different published series of adenomyomas also include cases with cystic spaces,21 adenomyomas with cystic degeneration,28 cystic adenomyosis,22 and extrauterine uterine-like masses.29 Other published cases of uterine-like masses correspond to cavitated rudimentary uterine horns,30 or possibly complex genital malformations with uterus didelphys and unilateral cervicovaginal atresia.25
Oliver6 reported in The Lancet, in 1912, a case of a 34-year-old woman with two children with an accessory uterus distended with menstrual fluid enucleated from the substance of the right broad ligament that extended close to the right round ligament of the uterus. But these uterine-like masses and those published as “isolated adenomyotic cysts” without adenomyosis uteri are rare,4 and they are generally observed in young and nulliparous women. However, the adenomyotic cyst in association with diffuse adenomyosis uteri is usually observed in women who are parous and older. There have been discussions on the criteria distinguishing cystic adenomyoma from adenomyotic cyst, but the attempt to differentiate the two types of uterine cysts appears to be meaningless.4 As observed in the cases reported here, the characteristics of the accessory and cavitated uterine masses are different from the true cystic adenomyomas associated with adenomyosis.
However, the majority of cases presenting an accessory and cavitated uterine mass are particularly difficult to differentiate from a functioning rudimentary uterine horn in a bicornuate uterus. Tamura et al2 also suggested that the differential diagnosis of an isolated adenomyotic cyst must include bicornuate uterus. Even when using magnetic resonance imaging, it is difficult to differentiate from a cavitated noncommunicating rudimentary uterine horn.16 However, the hysterosalpingogram is very useful for distinguishing it from a uterine anomaly. Most published cases showing a cavitated uterine horn correspond to a noncommunicating rudimentary and cavitated uterine horn with unicornuate uterus present on the contralateral side (American Society for Reproductive Medicine classification, type IIb), which is sometimes published as a uterine-like mass of the ovary.30 In addition, that cavitated uterine horn sometimes corresponds to segmentary atresias.31 In these cases, menstruation drains in a retrograde fashion, potentially causing endometriosis or provoking a critical and painful condition when a tubal sterilization is performed on the corresponding fallopian tube. However, the noncommunicating accessory uterine cavities are truly what their name implies, and they present clinically with painful symptoms from the beginning. Other cases that we think are likely to correspond to a hemiuterus with unilateral cervicovaginal atresia (uterus didelphys)25,32 also have been referred to as uterine-like masses.
As noted, Potter and Schenken1 reported a noncommunicating accessory uterine cavity in a 15-year-old nulligravida girl with a 1-year history of increasing dysmenorrhea. The accompanying illustration and coronal sonographic view of the uterus seemed consistent with our four cases and with the cases previously published as “isolated adenomyotic cyst.” Therefore, we think that all of these cases present with the same pathology: an accessory and cavitated noncommunicating uterine mass with functioning endometrium associated with an otherwise normal uterus. Clinically (and also histologically), these cases seem different from the cavitated adenomyomas associated with severe adenomyosis and leiomyomas in postmenopausal women. The former would represent an isolated anomaly of the Müllerian ducts and would therefore be a Müllerian malformation, whereas the latter would probably represent the evolution of severe adenomyosis.
In the evolutionary embryological development of the female genital tract, some mesonephric remnants may exist far away from the course of the ducts, especially in the vaginal wall, which can occasionally give rise to Gartner cysts. Thus, Müllerian remnants that lead to noncommunicating accessory uterine cavities associated with a normal uterus may develop in the same manner as a rudimentary uterine mass or appendix. However, it is interesting to note that our four cases and all published cases of juvenile cystic adenomyomas or noncommunicating accessory uterine cavity with an otherwise normal uterus are always located in the insertion area or pathway of the round ligament from the uterine horn, most frequently on the right. Therefore, it is probable that some relationship exists with the attachment of the gubernaculum during the embryological development of the uterus. Thus, their origin might be a dysfunction of the female gubernaculum.
From the histological viewpoint, Figure 4 shows that the accessory uterine horns have a thick myometrial wall without evidence of adenomyosis and with a cavity lined by an endometrial epithelium, unlike the cavitated adenomyoma without endometrial epithelium lining, which is shown in Figure 5. From the clinical viewpoint, severe dysmenorrhea can be attributable to a progressive increase in the size of the mass, the noncommunicating uterine cavity, stretching of the endometrial cavity, and intracystic bleeding.23
From the perspective of transvaginal ultrasound diagnosis, the accessory and cavitated uterine mass is clearly seen as a small endometrial cavity. This cavity raises a differential diagnosis that includes the cavitated rudimentary uterine horns observed in other malformations, although both types of cavities could coexist. Sometimes, the accessory endometrial cavity is larger and includes an endometriomalike structure with anterouterine and extraovarian locations.
In summary, noncommunicating accessory uterine cavities and juvenile or isolated cystic adenomyomas correspond to the same pathology: an accessory and cavitated uterine mass with an otherwise normal uterus. They are unusual Müllerian anomalies that cause severe dysmenorrhea and abdominal pain in young women. They are lined by endometrial epithelium and present as similar to the cavitated true adenomyomas. This latter pathology is observed in older women with severe adenomyosis, and the endometrial lining is generally absent. To rule out the diagnosis of a cavitated noncommunicating rudimentary uterine horn, magnetic resonance is useful, but the hysterosalpingogram showing a normal eutopic uterine cavity is decisive. Accessory uterine masses could be attributable to duplication and persistence of a Müllerian duct segment in a critical area at the level of the attachment of the round ligament, possibly related to a gubernaculum dysfunction.
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