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Diagn Pathol. 2012; 7: 117.
Published online 2012 Sep 3. doi:  10.1186/1746-1596-7-117
PMCID: PMC3487803

Microscopic endometrial perivascular epithelioid cell nodules: a case report with the earliest presentation of a uterine perivascular epithelioid cell tumor



Perivascular epithelioid cell (PEC) tumors (PEComas) are a family of related mesenchymal tumors composed of PECs which co-express melanocytic and smooth muscle markers. Although their distinctive histologic, immunohistochemical, ultrastructural, and genetic features have been clearly demonstrated, their histogenesis and normal counterpart remain largely unknown. Precursor lesions of PEComas have rarely been reported. We herein describe a tuberous sclerosis patient with microscopic PEC nodules in the endometrium of adenomyosis, pelvic endometriosis, an ovarian endometriotic cyst, and the endometrium of the uterine cavity. The nodules showed a mixture of spindle-shaped and epithelioid cells concentrically arranged around small arteries. The cells exhibited uniform nuclei, light eosinophilic cytoplasm, and immunoreactivity with HMB-45 and CD10. Some nodules revealed continuity with a PEComa in the myometrium. These findings support microscopic endometrial PEC nodules possibly being precursor lesions of uterine PEComas. The wide distribution of the nodules in the pelvis may be related to the multicentricity of PEComas in tuberous sclerosis patients. Owing to the immunoreactivity with CD10, microscopic endometrial PEC nodules may be misinterpreted as endothelial stromal cells unless melanocytic markers are stained. To the best of our knowledge, this is a case with the earliest manifestation of PEC lesions occurring in the endometrium.

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Keywords: Perivascular epithelioid cell, PEComa, Lymphangioleiomyomatosis, CD10, Adenomyosis, Endometriosis, Tuberous sclerosis


Neoplasms with perivascular epithelioid cell (PEC) differentiation (PEComas), as defined by the World Health Organization, are a family of mesenchymal tumors composed of histologically and immunohistochemically distinctive PECs, characteristically expressing both melanocytic and smooth muscle markers [1]. The concept of “PEC’ was first proposed by Bonetti et al. to identify a novel cell type, which exhibited an epithelioid appearance, clear-eosinophilic cytoplasm, and a perivascular distribution in renal angiomyolipoma (AML), clear-cell sugar tumor (CCST) of the lung, and lymphangioleiomyomatosis (LAM) [2]. Since that time, PEComas have been reported at a wide variety of anatomic sites [3-5]. In the female genital tract, PEComas most frequently affect the uterus [6]. AML, LAM, sclerosing PEComa, and PEComa-not otherwise specified (NOS) were described in the uterus [6-16]. We herein report a unique case of microscopic endometrial PEC nodules, which have never been reported in the literature, and they perhaps represent the earliest manifestation of uterine PEComas. We discuss their histologic and immunohistochemical features, the relationship between the microscopic PEC nodules and PEComas of the female genital tract, and their clinical significance.

Case presentation

Clinical summary

A 29-year-old woman had suffered from abnormal vaginal bleeding and severe dysmenorrhea for a long time. Urinary frequency was noted, with exacerbation during menstruation. The patient was known to have tuberous sclerosis which presented with epilepsy and adenoma sebaceum when she was 19 years old. She underwent a left nephrectomy for renal cell carcinoma and a right partial nephrectomy for AML at 20 years old. Ultrasonography showed a poorly demarcated heterogeneous area measuring 4.7 cm in the largest dimension in the myometrium. Debulking surgery for adenomyosis, ablation of the pelvic endometriosis, and cystectomy of the left ovary were performed. Two years later, the patient still complained of dysmenorrhea and diarrhea aggravated during menstruation. She received a second surgery with a clinical diagnosis of endometriosis. The gynecologist found severe fibrous adhesion and endometriosis in the pelvic cavity. A supracervical hysterectomy and bilateral salpingo-oophorectomy were performed. The follow-up information revealed no evidence of recurrent or metastatic disease 168 months after the hysterectomy.

Materials and methods

Specimens of the first surgery included two myometrial fragments, one piece of pelvic soft tissue, and some ovarian fragments. Specimens of the second surgery included the uterine corpus, bilateral ovaries, and bilateral fallopian tubes. All specimens were fixed in 10 % formalin and processed for a histologic examination by conventional methods. Hematoxylin and eosin (H&E)-stained sections were analyzed. Immunohistochemistry was performed using a Benchmark XT automated slide stainer (Ventana Medical Systems, Tucson, AZ, USA). The primary antibodies are listed in Table 1.

Table 1
Antibodies used in this study

Pathologic findings

On macroscopic examination, both myometrial fragments of the first surgery and the subsequently excised uterine corpus showed hypertrophic myometrium with trabecular cut surfaces. Tiny depressed hemorrhagic spots were observed. The uterine corpus measured 5.0 x 5.0 x 4.0 cm and was mildly enlarged. Fibrosis and extensive hemorrhage were observed on the serosa. One 0.8-cm myoma-like nodule with a well-demarcated margin was found within the myometrium. No thickening of the endometrium was seen. Histologically, the uterine corpus revealed adenomyosis throughout the entire myometrium, extending to the serosal surface (Figure (Figure1A).1A). A PEComa-NOS, composed of ill-defined spindle cell fascicles, was found to mainly be distributed around the adenomyosis foci (Figure (Figure1A).1A). In contrast to the deeply eosinophilic hypertrophic myometrium, the spindle cells had clear to lightly eosinophilic cytoplasm. Their nuclei were oval to spindle-shaped and uniform, with no mitotic activity. The endometrial stroma of adenomyosis was focally replaced by the PEComa. LAM, characterized by poorly defined nodular proliferation of spindle cell fascicles with many tongue-like protrusions in dilated vascular spaces, was also noted in the myometrium (Figure (Figure1B).1B). Tumor cells of the PEComa and LAM showed diffuse immunoreactivity with smooth muscle actin (SMA) and progesterone receptor (PR) (Figure (Figure1D,1D, E, G, H). HMB-45 and desmin were expressed to a lesser degree. They were negative for CD10 and estrogen receptor (ER). The myoma-like nodule was a sclerosing PEComa with uniform epithelioid cells in a hyalinized extracellular matrix (Figure (Figure1C).1C). It showed focal HMB-45, PR, SMA, and desmin expressions (Figure (Figure1F,1F, I). Neither CD10 nor ER expression was observed. Ovarian and pelvic tissues, taken during the first surgery, respectively revealed an endometriotic cyst and endometriosis.

Figure 1
Adenomyosis-associated perivascular epithelioid cell tumor (PEComa), lymphangioleiomyomatosis, and sclerosing PEComa (x100). (A) An adenomyosis-associated PEComa with ill-defined tumor borders and light eosinophilic tumor cells (arrow). The PEComa was ...

In addition to the PEComas and LAM, microscopic nodules composed of spindle-shaped to epithelioid cells, which were concentrically arranged around spiral arteries, were easily apparent within the ectopic endometrium of the adenomyosis (Figure (Figure2A-C).2A-C). These nodules measured < 1 mm in maximal dimension. Some of them were confined within the endometrium despite serial sections, whereas others had continuity with the PEComa in the myometrium. The spindle-shaped and epithelioid cells had indistinct cell borders, light eosinophilic cytoplasm, uniform nuclei, and no mitotic activity. They showed diffuse and strong immunoreactivity for HMB-45, CD10, and PR (Figure (Figure2D-F).2D-F). Immunoreactivity with SMA was rarely seen. Desmin and ER expressions were not detected. On the basis of the histological and immunohistochemical findings, the microscopic nodules also represented PEC lesions. Identical nodules, highlighted by HMB-45 immunostaining, were occasionally found in the ectopic endometrium of the left ovary, the pelvic endometriosis, and the basal layer of the endometrium in the uterine cavity, although they were inconspicuous on H&E-stained sections (Figure (Figure33A-D).

Figure 2
Histologic and immunohistochemical features of microscopic perivascular epithelioid cell (PEC) nodules in the endometrium of adenomyosis. (A) Microscopic PEC nodules in the endometrium of adenomyosis (arrowhead). Note the PEC tumor (PEComa) in the myometrium ...
Figure 3
Microscopic perivascular epithelioid cell (PEC) nodules in the endometrium of an endometriotic cyst and uterine cavity (x400). (A) Microscopic PEC nodules in the endometriotic cyst (arrowhead) (hematoxylin-eosin). (B) HMB-45 immunostaining highlighting ...


Since HMB-45 immunoreactivity was described in renal AML and pulmonary CCST in 1991, the family of PEComas has expanded to include AML, LAM, CCST, clear-cell myomelanocytic tumor of the falciform ligament/ligamentum teres, and clear-cell tumors of other anatomic sites in the past 2 decades [1,17-21]. Although their distinctive morphologic, immunohistochemical, ultrastructural, and genetic features have been clearly demonstrated, their histogenesis and normal counterpart remain poorly understood [4]. Rare examples of early or precursor lesions of PEComas were reported in the literature [11,12,22-25]. In the current case, some microscopic PEC nodules, which were entirely confined within the endometrium with no attachment to the myometrium or the PEComa despite serial sections, were seen. These findings indicate that the nodules were not a consequence of an infiltration from the PEComa in the myometrium, supporting such nodules representing an example of early or precursor PEC lesions. We speculate that a uterine PEComa may evolve from these nodules. Proliferation of PECs initially begins around small arteries in the endometrium and produces microscopic PEC nodules. Further proliferation of PECs expands the nodule size and subsequently extends to the myometrium forming a better-developed PEComa. Only three other cases with similar early or precursor PEC lesions were reported in female genital organs, with two cases being associated with uterine PEComas and the other regarded as the earliest LAM [11,12,22]. The authors used the designation ”PEComatosis” to describe such lesions [11,12]. The clinical and pathologic features of these cases, including ours, are summarized in Table 2. The size of the early or precursor PEC lesions was usually < 2 mm. All cases, except the case reported by Liang et al., showed a similar immunohistochemical profile with diffuse positivity to melanocytic markers and focal positivity to smooth muscle markers. The case described by Liang et al. also revealed positive immunoexpressions for HMB-45 and SMA, but the extent of the staining was not described. Involvement of early PEC lesions in multiple organs was found in three patients, all of whom were complicated with tuberous sclerosis. The phenomenon may simply reflect the underlying genetic alterations associated with tuberous sclerosis, in which simultaneous or non-simultaneous development of multiple PEComas in many organs is characteristic [5]. Although patients with tuberous sclerosis are prone to having multiple PEComas and/or early PEC lesions in the female genital tract, the multicentricity of PEComas does not seem to be associated with adverse clinical outcomes [11,16]. Our patient remained free of local recurrence and metastasis 168 months after excision of the uterine corpus, ovaries, and fallopian tubes.

Table 2
Early or precursor perivascular epithelioid cell lesions reported in the uterus

AMLs, the most common member of PEComas, were reported to have similar early PEC lesions, which were designated as microharmatomas, small mesenchymal nodules, or intraglomerular lesions [4,23-25]. Such lesions were confined within glomeruli or located outside glomeruli. They contained only epithelioid cells or a mixture of epithelioid cells and adipocytes. Immunoreactivity with HMB-45 was consistently noted in epithelioid cells. Chowdhury et al., analyzing the histologic relationship between small mesenchymal nodules and AML, found that small-sized mesenchymal nodules tended to only be comprised of epithelioid cells without adipocytes or blood vessels, compared to large-sized ones which contained epithelioid cells, adipocytes, and blood vessels [24]. These findings support small mesenchymal nodules being the buds of AMLs. Precursor PEC lesions were also described in association with a urachal PEComa [26]. The precursor lesion, remote from the main urachal PEComa, was composed of capillaries lined by HMB-45-positive clear cells. A gradual transition from the precursor lesions to invasive PEComa nests was observed.

The present case is unique for the early PEC lesions being present in the endometrium, in contrast to other early PEC lesions, which were reported in the myometrium [11,12,22] (Table 2). The endometrial distribution of early PEC lesions may account for rare uterine PEComas, which present as polypoid endometrial lesions with minimal myometrial involvement [9,10]. This also strengthens the supposition that uterine PEComas are distinctive from uterine smooth muscle tumors. Uterine PEComas being a distinct clinicopathologic entity can be challenged by frequent HMB-45 expression in epithelioid and conventional leiomyosarcomas of the uterus [27-29]. The question arises as to whether uterine PEComas are a distinctive entity or whether they represent a subgroup of HMB-45-positive smooth muscle tumors [30]. Since smooth muscle tumors typically originate in the myometrium, the endometrial origin of early PEC lesions supports uterine PEComas being a distinctive tumor. The immunophenotype of early PEC lesions, with diffuse HMB-45 and rare SMA expressions, also argues against their origin from smooth muscle cells.

Another immunophenotypic feature requiring further discussion is CD10 expression. In the present case, CD10 expression was restricted to microscopic endometrial PEC nodules, whereas the well-formed PEComa, LAM, and sclerosing PEComa in the myometrium showed negative CD10 reactivity. CD10 expression was reported in 25 % of uterine PEComas which underwent CD10 staining [6]. Although CD10 reactivity is not low in uterine PEComas, the significance of CD10 expression remains to be elucidated. Herein, we try to clarify the role of CD10. First, CD10 is commonly used to distinguish endometrial stromal nodules/sarcomas from uterine smooth muscle tumors [31]. CD10, although occasionally positive in smooth muscle tumors, is relatively specific for endometrial stromal cells. It would be interesting to determine whether or not the development of uterine PEComas is related to endometrial stromal cells. In CD10-positive uterine PEComas, tumor locations were not limited to the endometrium [10,32,33]. CD10 expression was not always detected in uterine PEComas which extensively involved the endometrium [13]. On the basis of the aforementioned findings, the hypothesis that uterine PEComas are derived from endometrial stromal cells is not supported. Second, CD10 is used as a cell surface marker of mesenchymal stem cells and tumor stem cells [34]. It is of paramount importance to understand whether CD10 is a surface marker of tumor stem cells of uterine PEComas. Unfortunately, CD10 is not routinely used in diagnosing PEComas. CD10 staining was not done in the other uterine PEComas with early or precursor PEC lesions [11,12]. More cases with early or precursor PEC lesions stained with CD10 are required to answer this question.

Moreover, since uterine PEComas may present as endometrial lesions with CD10 expression, PECs may be misinterpreted as endometrial stromal cells, particularly in an endometrial curettage specimen. Plump cells with more abundant clear to light eosinophilic cytoplasm and a radial arrangement around vessels should raise suspicion of the existence of PECs. A misdiagnosis can be avoided by awareness of the existence of endometrial PEComas and assistance with immunostaining using melanocytic markers.


The present case showed microscopic endometrial PEC nodules widely distributed in the endometrium of adenomyosis, pelvic endometriosis, an ovarian endometriotic cyst, and the endometrium of the uterine cavity in a tuberous sclerosis patient. The microscopic endometrial PEC nodules were clearly demonstrated to have progressed into a uterine PEComa. Further studies focusing on early HMB-45-positive PEC nodules may be helpful in clarifying the pathogenesis of PEComas. The role of CD10 in PEComas also needs to be further evaluated.


Written informed consent was obtained from the patient for publication of this Case Report and all accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.


AML, Angiomyolipoma; CCST, Clear-cell sugar tumor; LAM, Lymphangioleiomyomatosis; PEC, Perivascular epithelioid cell; PEComa, Perivascular epithelioid cell tumor.

Competing interests

The authors declare that they have no competing interests.

Authors’ contribution

CLF participated in drafting the manuscript and reviewing the literature. CLF, YHL, and WYC were responsible for making the pathologic diagnosis. WYC proposed the idea and revised the manuscript. All authors have read and approved the final manuscript.


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