Introduction

Adenomatoid tumors (ATs) are relatively rare benign lesions that are reported most commonly in the genital tracts of both sexes, including the paratesticular structures in males, and the uterus, fallopian tubes, and ovaries in females [1]. These tumors occur much less frequently in extragenital locations but have been described in various organs and anatomic sites, including the mesentery [2], mediastinum [3], pleural cavity [4], adrenal glands [5], pancreas [6], heart [7], and mediastinal lymph nodes [8]. In a few reported cases, ATs involved several anatomic sites simultaneously; e.g., the uterus, ovaries, and appendix [9]. Here we report a case of AT involving the uterus and its regional lymph nodes. To our knowledge, this is the first report of uterine AT simultaneous involvement of regional lymph nodes.

Case report

A 49-year-old nonparous female presented to her primary care physician complaining of menorrhagia. She had a previous history of secondary hydrocephalus and left ovarian cystectomy but the details were unknown. Computed tomography (CT) revealed an enlarged uterus with a lobulated low attenuation mass of maximum diameter 10 cm embedded in the right posterior myometrium. On magnetic resonance imaging (MRI), T2-weighted images (T2WI) showed a high intensity septated multicystic mass protruding from the myometrium (Fig. 1a,d). The cystic components showed low intensity on T1-weighted images (T1WI) (Fig. 1b). The septa showed isointensity on T1WI and T2WI to that of myometrium, and slight enhancement on post-contrast fat-saturated T1WI (Fig. 1c). No area of significant high intensity was observed on diffusion-weighted imaging (DWI) (Fig. 1e). The bilateral obturator and right common iliac lymph nodes were enlarged (diameter 1–1.5 cm) and contained solid and multicystic components, the same as the uterine mass (Fig. 1g). FDG PET/CT was performed to investigate lymph node involvement and showed minimal FDG uptake in the uterus and lymph node lesions (Fig. 2). Based on the radiologic findings, the differential diagnoses included leiomyoma, endometrial stromal sarcoma, myxoid leiomyosarcoma, and adenomatoid tumor. The patient underwent surgical resection for preoperative diagnosis of malignancy involving regional lymphadenopathy, and total hysterectomy, bilateral salpingo-oophorectomy, and pelvic lymph node biopsy were performed. Examination of hematoxylin-eosin-stained permanent sections of the uterine lesion revealed a neoplasm characterized by pseudoacini and anastomosing channels lined by both epithelioid and flattened cells (Fig. 3a,b). The migration of the mucin into the interstitium was observed (Fig. 3a). The epithelioid and flattened cells exhibited strong immunoreactivity for calretinin (Fig. 3c), CAM 5.2, and D2-40, but were estrogen-receptor- and progesterone-receptor-negative, and were also negative for desmin, αSMA, and CD34. Examination of hematoxylin-eosin-stained permanent sections of the bilateral obturator lymph nodes revealed variably dilated acinar structures (Fig. 3d). Immunostaining of the lymph node lesions showed strong immunoreactivity of calretinin and D2-40, the same as the uterine lesion. Hematoxylin-eosin histology and immunophenotyping confirmed the mesothelial differentiation of the neoplasm. AT involving the uterus and lymph nodes was diagnosed.

Fig. 1
figure 1

Contrast-enhanced MRI. a Sagittal T2WI, b sagittal T1WI, c sagittal post-contrast fat-saturated T1WI, d axial T2WI, e axial DWI (b = 1000), f axial ADC map, g coronal fat-saturated T2WI. MRI showed aggregated cystic mass located in the uterine posterior wall. The mass showed high intensity on T2WI and mix intensity of low and intermediate on T1WI. The septa showed isointensity on T1WI and T2WI to that of myometrium, and slightly enhancement on post-contrast fat-saturated T1WI. A part of the tumor protruded outside the uterus (arrow in d). Signal intensity of the tumor on DWI was intermediate with its ADC map high. Bilateral obturator and right common iliac lymph nodes lesions had same characteristic as uterine lesion (arrows in g)

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Fig. 2
figure 2

a and b FDG PET/CT revealed minimal FDG uptake in the uterus and lymph node lesions (arrow)

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Fig. 3
figure 3

a–d Histopathological images of AT (a, b, HE staining of uterine lesion, c calretinin staining of uterine lesion, d HE staining of lymph node lesion). The uterine tumor showed pseudoacini and anastomosing channels lined by both epithelioid cells and flattened cells with emigration of mucus to the interstitium. The cells lining the cystically dilated spaces showed positive immunostaining for calretinin. The lymph node tumor showed honeycomb arrangement of cystic spaces lined by a single layer of flattened cells, which showed positive immunostainig for calretinin

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Discussion

The term “adenomatoid tumor” was first introduced in 1945 by Golden and Ash [10] to describe benign lesions that display a strikingly adenomatous appearance. ATs are commonly asymptomatic and found incidentally [10,11,12]. The most common sites of involvement are the epididymis in men, and the fallopian tubes and uterus in women [10, 12, 13]. Adenomatoid tumors of epididymis shows low intensity relative to testicular parenchyma on T2WI. These tumors demonstrate slow or decreased contrast enhancement relative to the testicular parenchyma or contralateral testis. However, the enhancement can be variable because, less commonly, adenomatoid tumors show hyperenhancement relative to the testis [14]. Rarely, these tumors may originate in extragenital sites, such as the mesentery [2], mediastinum [3], pleural cavity [4], adrenal glands [5], pancreas [6], heart [7], and mediastinal lymph nodes [8].

The histogenesis of ATs is controversial, and mesonephric, Müllerian, endothelial, and mesothelial origins have all been suggested. Mesothelial cells have been proposed as the progenitor cells of these tumors [11, 12].

Histologically, ATs can be classified as adenoid, angiomatoid, solid, or cystic type [13, 15,16,17]. One pattern may predominate, but an admixture of two patterns is more common, with the most frequent combination being adenoid and angiomatoid. The cystic type of AT is the least common. It has been the subject of mostly single case reports [1, 15,16,17,18] and is the histological pattern found in the uterine and lymph node lesions of the present patient.

Uterine AT can be found in 0.12–1.2% of all women [13, 19]. The actual incidence is probably higher; these tumors frequently go undetected because of their small size and gross appearance, which is similar to that of leiomyoma [20, 21]. They occur most often in women of reproductive age. A previous study has reported a mean age of 41 years (range 26–55 years) at initial diagnosis [22]. The clinical manifestations of uterine AT are nonspecific and variable, and include vaginal bleeding, menorrhagia, and abdominal masses [23]. Most uterine ATs present as a subserosal mass located near the uterine horn [16]. They are often solitary and small, with a mean diameter of 2.1 cm (range 2–10 cm) [17]. On gross examination, ATs are soft and moist, and may have mucus degeneration. They can show an invasive growth pattern due to the lack of a capsule [24]. The radiologic findings of the present uterine lesion were typical of a cystic adenomatoid mass. Based on the radiologic findings, as a cystic mass forming in the uterine corpus, we differentiated leiomyoma, endometrial stromal sarcoma, myxoid leiomyosarcoma, and AT. Leiomyomas are by far the most common uterine tumors and the most common gynecologic tumors. 4% of leiomyomas undergo cystic degeneration, with extensive edema forming cystic, fluid-filled spaces [25]. Endometrial stromal sarcomas account for 10% of primary uterine sarcomas. Although they commonly appear as a polypoid mass, Park et al. reported that low-grade endometrial stromal sarcomas showed multiseptated cystic appearance (20%) or a multiple clustered small cystic appearance (30%) [26]. Rarely, myxoid leiomyosarcoma can be showed same radiologic findings [27], it is difficult to differentiate these from AT, signal intensity of diffusion-weighted image might be the key to distinguish AT from other tumors especially malignancies as endometrial stromal sarcomas and myxoid leiomyosarcomas.

Although multiple tumors in the genital tract have previously been reported as rare (2.8%) [28], a recent report stated that their occurrence is not uncommon (20%) [22]. Most previous reports describe multiple ATs restricted to the uterine corpus. Srigley reported a rare case of multifocal and diffuse ATs involving the uterus and a fallopian tube [29], and Harada reported a rare case of ATs in three different anatomical sites: the uterus, right ovary, and appendix [9].

Isotalo et al. reported AT in a mediastinal lymph node [8], which to the best of our knowledge is the first and only previous description of AT involving lymph nodes. However, there are several reports of hyperplastic mesothelial cells in lymph nodes [30, 31]. It has been suggested that ATs that develop in nonmesothelial-lined sites such as the lymph nodes may have originated from mesothelial inclusions [5] or even from embolized mesothelial cells [30, 31]. Our patient had ATs involving the uterus and its regional lymph nodes. This case supports the hypothesis of AT development from embolized mesothelial cells that originated in the uterus.

The treatment for uterine AT is surgical resection, by hysterectomy or laparoscopic tumor excision. The prognosis is good, and no cases of recurrence or metastasis have been reported in the literature. Careful follow-up and management is recommended in the present case because of the lymph node involvement.

In summary, we report a case of uterine AT simultaneous involvement of regional lymph nodes. Although the radiologic findings of uterine AT of our case quite match the character of cystic type uterine AT, differential diagnosis must be done to distinguish AT from malignancy, in terms of involvement of regional lymph nodes.