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13 October 2022: Articles  Japan

Successful Surgical Treatment of a Recurrent Pelvic Solitary Fibrous Tumor of Uterine Origin Accompanied by Doege-Potter Syndrome: A Case Report

Mistake in diagnosis, Rare disease

Yasunori Deguchi1ABCDEF*, Wataru Komuta1BCDEF, Tomokazu Watanabe2BCD, Kazuho Saiga3BCD, Koki Kurahashi1B, Kazuo Otsuka1B, Koji Hirata1B, Masaki Mizumoto1B, Akihiro Kitaoka1B, Masazumi Zaima1ABE

DOI: 10.12659/AJCR.936806

Am J Case Rep 2022; 23:e936806

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Abstract

BACKGROUND: Solitary fibrous tumors (SFT), rare soft-tissue neoplasms, are usually found in the thoracic cavity, and a uterine origin is extremely rare. SFTs with insulin-like growth factor-II (IGF-II) production induce non-islet cell tumor-induced hypoglycemia (NICTH), referred to as Doege-Potter syndrome.

CASE REPORT: A 70-year-old woman presented with urinary retention, and imaging revealed a huge mass occupying almost the entire pelvic space. She had a history of hysterectomy for leiomyoma of the uterus 7 years earlier. In her present course, she developed hypoglycemia, and NICTH was suspected. Her previous uterine specimen was reexamined, and immunohistochemistry (IHC) revealed the specimen to be CD34-positive and alpha-smooth muscle actin-negative, indicating that the uterine specimen was not leiomyoma but SFT. Therefore, the present pelvic tumor was considered to be a recurrence of SFT with NICTH, namely Doege-Potter syndrome. Surgical resection was performed, and the pathological examination showed the same histologic features as the previous uterine specimen, while IHC revealed the present specimen to be positive for CD34, signal transducers and activator of transcription 6, and IGF-II, consistent with the diagnosis of recurrent SFT with IGF-II production. The patient’s hypoglycemia improved after tumor resection. To confirm the IGF-II secretion from the SFT, we conducted immunoblotting of the patient’s perioperative serum, with results showing that the strong band of IGF-II in the preoperative serum disappeared after surgery.

CONCLUSIONS: Because SFTs, especially those with Doege-Potter syndrome, often recur, sometimes with a very long interval, long-term cautious surveillance is required, even after complete tumor resection.

Keywords: Hypoglycemia, Insulin-Like Growth Factor II, Solitary Fibrous Tumors, Uterus

Background

Solitary fibrous tumors (SFTs) are rare mesenchymal fibroblastic neoplasms that develop mostly in the thoracic cavity [1]. Although extra-thoracic SFTs have been increasingly reported, such as in the pelvic space [1–7], SFTs of a uterine corpus origin are extremely rare [8–13]. Ardighieri et al performed a systematic literature review, and found only 13 SFTs of a uterine corpus origin had been reported in the English-language literature [11]. They noted that most patients presented with local symptoms related to a leiomyoma-like mass, such as abnormal uterine bleeding, abdominal fullness, or a palpable mass; furthermore, all patients underwent surgical resection, and 10 patients who had data available were all alive at 6 to 56 months of follow-up, while 2 patients had developed metastases or local recurrence.

Approximately 4% to 11.5% of patients with SFT develop non-islet cell tumor-induced hypoglycemia (NICTH) by secreting high-molecular-weight (HMW) insulin-like growth factor-II (IGF-II), which is referred to as Doege-Potter syndrome. The predominant symptom of Doege-Potter syndrome is severe and refractory hypoglycemia, and hypoglycemic symptoms can sometimes be the initial indicator that leads to the detection of a large tumor by imaging studies and ultimately the diagnosis of an SFT [14,15].

We report a case of recurrent SFT of uterine origin accompanied by Doege-Potter syndrome that was successfully treated with surgical resection.

Case Report

The patient was a 70-year-old woman who had a history of total hysterectomy with bilateral salpingo-oophorectomy for uterine leiomyoma 7 years earlier. She presented to our hospital with a concern of urinary retention. Contrast-enhanced computed tomography (CT) revealed a huge hypervascular tumor occupying most of the pelvic space, compressing the bladder and rectum (Figure 1), and she was admitted to our hospital. She was on medication for hypertension and osteoporosis and had no other relevant medical history. About 1 month after her presentation, she felt nocturnal weakness and fatigue every night that lasted until early in the morning, symptoms that were found to be indicative of hypoglycemia.

At admission, her abdomen was slightly swollen, but she had no abdominal pain or tenderness. A laboratory examination at admission showed hypoglycemia (39 mg/dL) and suppressed serum insulin (<2.0 µU/mL) and C-peptide (0.09 mg/mL), but no anti-insulin antibody. A CT scan showed an almost 12-cm-diameter solid mass with heterogenous enhancement in the pelvic space that was compressing the bladder and rectum to the right (Figure 1A). Magnetic resonance imaging (MRI) showed that the mass was composed of a low-intensity area on T1-weighted imaging (Figure 1B) and a heterogenous isoto high-intensity area on T2-weighted imaging (Figure 1C).

Because she developed hypoglycemic symptoms at night despite a low insulin level, NICTH was suspected and the uterus specimen of 7 years ago was reexamined. Grossly, the tumor was well circumscribed and elastic and firm, and the cut surfaces were yellow to brown in color. Microscopically, the tumor cells were spindle-shaped and had a patternless arrangement, with collagenous stroma and irregularly dilated vasculature. The tumor cells showed moderate atypia, and the mitosis index was 1 mitosis per 10 high-power fields (HPFs) (Figure 2A). Immunohistochemistry (IHC) revealed that the specimen was CD34-positive but negative for alpha-smooth muscle actin (SMA), c-kit, S100, and myoglobin, findings that led to the correct diagnosis of the uterus tumor as SFT instead of leiomyoma (Figure 2B, 2C). Therefore, the present pelvic tumor was considered to be the recurrent tumor of the uterus SFT producing IGF-II, resulting in hypoglycemia.

It took time to conduct preoperative investigations and to prepare for the operation because of the COVID-19 pandemic; therefore, about 1.5 months after her first presentation, tumor resection was scheduled following continuous glucose infusion. During laparotomy, disseminated tumors were found, and the main pelvic tumor had severely adhered to the rectum and left ureter. Tumor resection, including excision of all visible disseminated tumors with combined resection of the rectum (low anterior resection) and left ureter (accompanied with ureteroneocystostomy), was performed. The operation time was 567 min, intraoperative blood loss was 2925 g, and 1560 mL of blood transfusion was performed. The main tumor measured 19 cm in maximum diameter and weighed 1050 g (Figure 3A). The tumors were solid and elastic soft, and their cut surfaces were yellowish- to grayish-white in color (Figure 3B). Pathologically, similar to the previous uterine specimen, the tumor was mainly composed of haphazardly arranged spindle cells with dilated and staghorn-shaped vasculature and partially necrotic lesions. Tumor cells were denser than in the previous uterine specimen, showing moderate atypia, and the mitosis index was 1 mitosis per 10 HPFs (Figure 4A, 4B). IHC revealed the tumor cells to be positive for CD34 (Figure 4C), signal transducers and activator of transcription 6 (STAT6) (Figure 4D), and IGF-II (Figure 4E) and negative for alpha-SMA, c-kit, and S100, consistent with the diagnosis of recurrent SFT with IGF-II production. The Ki67 index was 17% in the main tumor and 3% to 10% in the disseminated tumors (Figure 4F).

To support the diagnosis of Doege-Potter syndrome, we conducted an immunoblotting analysis of the patient’s perioperative serum along with homogenized tumor tissue. Clear bands of HMW IGF-II (around 15 kDa) were detected in both the preoperative serum and tumor tissue, but they disappeared in the postoperative serum (Figure 5). The patient no longer had hypoglycemia after surgery.

A follow-up CT at 5 months after surgery showed a supposedly residual disseminated tumor at the bottom of the pelvis. As she refused re-operation because of her mental illness, which had developed due to postoperative stress disorder, cautious follow-up was conducted. The tumor size did not change during the follow-up; however, she ultimately died of a cause other than SFT 2 years after the surgery.

Discussion

We encountered a very rare case of “malignant” SFT of uterine corpus origin, which had been misdiagnosed as a leiomyoma. Ardighieri et al reported only 13 cases of SFTs of the uterine corpus in their systematic review, 2 of which had distant metastases or pelvic recurrence at over 6 to 56 months of follow-up [11]. Furthermore, only 1 of the 13 cases presented with hypoglycemia, making our case the first uterine corpus SFT case to recur after 7 years of follow-up, accompanied by Doege-Potter syndrome.

SFTs are histologically composed of spindled to ovoid cells with indistinct, pale eosinophilic cytoplasm within a variably collagenous stroma [16] and can mimic many unrelated mesenchymal and non-mesenchymal tumor entities [10,17]. CD34 is one of the most characteristic conventional IHC markers in SFTs, although gastrointestinal stromal tumors are also positive for CD34 and should be excluded [1,18]. Recently, strong nuclear STAT6 expression due to a NAB2-STAT6 gene fusion was identified as the most consistent and specific IHC marker of SFTs [19–21]. The 2020 WHO Classification of Soft Tissue Tumours describes that, in addition to the reported histological features, CD34 and/or STAT6 expression by IHC is essential for a diagnosis [16]. In addition to CD34 and STAT6, bcl2 and vimentin are usually immunoreactive in SFTs, whereas

SMA and desmin (myocyte marker), or S-100 and synaptophysin (perineural tissue marker), or c-kit (gastrointestinal stromal tumor marker) are negative [10,12,14]. Other histological differential diagnoses are synovial sarcoma or deep fibrous histiocytoma (which are both negative for CD34), or myopericytoma (which usually develops in the extremities and is positive for SMA). We probably would have detected the pelvic tumor much earlier at a much smaller size with close follow-up if the uterine tumor 7 years earlier had been precisely diagnosed as an SFT by IHC. The pathologist at that time most likely overlooked other possibilities in the differential diagnosis because leiomyomas are predominantly identified to be non-epithelial uterine tumors. As a result, the pathologist may have not considered IHCs to be required.

Doege-Potter syndrome is a paraneoplastic syndrome associated with SFTs, and its predominant symptom is severe and refractory hypoglycemia. Large SFTs (>20 cm) tend to present with this uncommon syndrome [14]. In patients with Doege-Potter syndrome, neoplastic cells of SFTs overexpress and secret HMW-IGF-II, which is insufficiently processed into IGF-II protein, resulting in NICTH [14,22]. The IHC of IGF-II is helpful for the diagnosis of Doege-Potter syndrome, while IGF-II overexpression does not always induce clinical hypoglycemia [14].

Several studies have confirmed the secretion of HMW-IGF-II using immunoblotting analyses of perioperative serum [15,22,23]. In the present case, an immunoblotting analysis revealed that the strong band of HMW-IGF-II in the preoperative serum had disappeared after tumor resection, which is compatible with the clinical improvement of hypoglycemia after surgery. The tumor size is reportedly related to IGF-II production, and over 90% of tumors greater than 9 cm in size have IGF-II overexpression [14]. In our case, the patient had not developed hypoglycemia until the recurrent tumor had grown to occupy the whole pelvic space.

Surgical resection has been the mainstay of SFT treatment. As SFTs are typically well-circumscribed masses and grow expansively, not invasively, complete tumor resection is usually possible. En bloc resection is not always required, and even piecemeal resection is acceptable for achieving good local control, resulting in a favorable prognosis [24]. However, repeated surgeries for recurrent SFTs or too-large tumors can cause distressful adhesion, and complete surgical resection is considerably challenging [15]. To avoid a positive surgical margin and reduce operative blood loss, several studies have reported the utility of preoperative transcatheter arterial embolization, as SFTs are usually hypervascular tumors [5,25]. In our case, the main pelvic tumor had grown so large that the tumor had severe adhesion to the rectum and the left ureter, so it might have been wise to consider preoperative transcatheter arterial embolization followed by surgery. Limited studies have additionally reported that systemic chemotherapy and radiotherapy are effective for SFT treatment. Further studies concerning the molecular pathways involved with SFTs are expected to highlight promising molecular targets [1].

For predicting the recurrence or metastasis of surgically resected SFTs, England’s pathologic criteria are well reported: size over 10 cm, increased cellularity, over 4 mitoses per 10 HPFs, nuclear pleomorphism, and tumor necrosis or hemorrhaging [26]. Even “benign” SFTs that do not meet England’s criteria are often reported to recur, and recently several risk factors in addition to England’s criteria have been proposed, such as an extrathoracic location [27,28]. Furthermore, SFTs with Doege-Potter syndrome are known to be much more malignant than those without Doege-Potter syndrome, and indeed, Han et al reported that as many as 60% of SFTs with Doege-Potter syndrome were malignant, compared with only 5% to 10.4% of those without the syndrome [14]. In addition, it should be noted that SFTs sometimes recur many years after the initial surgery [15,29]. In our present case, because the patient had a huge SFT tumor over 10 cm in size accompanied by Doege-Potter syndrome and already had disseminating tumors, the risk of recurrence was considered very high, so we intended to cautiously conduct follow-up, but she unfortunately died of a cause other than SFT recurrence.

Conclusions

We reported a very rare case of recurrent SFT of uterine origin with Doege-Potter syndrome. We confirmed that the tumor cells had produced and secreted IGF-II and that the serum IGFII had dramatically decreased after tumor resection. Because SFTs, especially those with Doege-Potter syndrome, often recur, sometimes with a very long interval, long-term cautious surveillance is required, even after complete tumor resection.

Figures

Figure 1.. Computed tomography (CT) and magnetic resonance imaging (MRI) at presentation. (A) Contrast-enhanced CT showed a heterogeneously enhanced mass occupying the pelvic space that compressed the bladder (yellow arrows) and the rectum (yellow arrow heads) to the right. (B) T1-weighted MRI showed a low-intensity mass. (C) T2-weighed MRI showed a heterogenous iso- to high-intensity mass. Figure 2.. Reexamination of the resected uterus specimen 7 years ago. (A) Hematoxylin and eosin staining. (B) Immunohistochemistry (IHC) study of CD34 showed diffusely positive staining. (C) IHC of alpha-smooth muscle actin showed that the tumor cells had negative staining (Scale bars: 100 µm). Figure 3.. Resected specimens of the present surgery. (A) The resected tumors had fibrous capsules. (B) The cut surfaces were yellowish- to grayish-white in color. Figure 4.. Pathological findings of the resected specimens. (A, B) Hematoxylin and eosin staining with a (A) low-power view and a (B) high-power view. (C–E) Immunohistochemistry (IHC) showed positive staining for CD34 (C), STAT6 (D), and IGF-II (E). (F) IHC study of Ki67 (Scale bars: 100 µm). Figure 5.. Immunoblotting of IGF-II for perioperative serum and resected specimen. The dense band at around 15 kDa (high-molecular-weight IGFII) in the patient’s preoperative serum (lane 1) disappeared in the patient’s postoperative serum (lane 2). The homogenized tumor tissue also had an IGF-II band (lane 3). NC – negative control; PC – positive control; ST – standard of this IGF-II antibody (7 kDa).

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Figures

Figure 1.. Computed tomography (CT) and magnetic resonance imaging (MRI) at presentation. (A) Contrast-enhanced CT showed a heterogeneously enhanced mass occupying the pelvic space that compressed the bladder (yellow arrows) and the rectum (yellow arrow heads) to the right. (B) T1-weighted MRI showed a low-intensity mass. (C) T2-weighed MRI showed a heterogenous iso- to high-intensity mass.Figure 2.. Reexamination of the resected uterus specimen 7 years ago. (A) Hematoxylin and eosin staining. (B) Immunohistochemistry (IHC) study of CD34 showed diffusely positive staining. (C) IHC of alpha-smooth muscle actin showed that the tumor cells had negative staining (Scale bars: 100 µm).Figure 3.. Resected specimens of the present surgery. (A) The resected tumors had fibrous capsules. (B) The cut surfaces were yellowish- to grayish-white in color.Figure 4.. Pathological findings of the resected specimens. (A, B) Hematoxylin and eosin staining with a (A) low-power view and a (B) high-power view. (C–E) Immunohistochemistry (IHC) showed positive staining for CD34 (C), STAT6 (D), and IGF-II (E). (F) IHC study of Ki67 (Scale bars: 100 µm).Figure 5.. Immunoblotting of IGF-II for perioperative serum and resected specimen. The dense band at around 15 kDa (high-molecular-weight IGFII) in the patient’s preoperative serum (lane 1) disappeared in the patient’s postoperative serum (lane 2). The homogenized tumor tissue also had an IGF-II band (lane 3). NC – negative control; PC – positive control; ST – standard of this IGF-II antibody (7 kDa).

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American Journal of Case Reports eISSN: 1941-5923
American Journal of Case Reports eISSN: 1941-5923