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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2023  |  Volume : 66  |  Issue : 1  |  Page : 135-140
A case of TFE3 translocation renal cell carcinoma with rare morphological features and literature review


1 Department of Pathology, The Affiliated Hospital of Southwest Medical University, Luzhou, China
2 Department of Medical Imaging, The Affiliated Hospital of Southwest Medical University, Luzhou, China
3 Department of Medical Ultrasound, The Affiliated Hospital of Southwest Medical University, Luzhou, China

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Date of Submission23-Jul-2021
Date of Decision15-Aug-2021
Date of Acceptance16-Aug-2021
Date of Web Publication18-Jan-2023
 

   Abstract 


Context: TFE3 translocation renal cell carcinoma (RCC) is a rare tumor that represents approximately 1% of RCC. It was classifed as a member of MiT family translocation RCCs by the World Health Organization in 2016. It is characterized by Xp11 translocation gene fusions involving TFE3. The diagnosis of TFE3 translocation RCC is based on immunohistochemical analysis and TFE3 break apart probes in FISH analysis, rather than histological characteristics and imaging examination. Aims: To determine the clinico-pathological, immuno-phenotypic, and cytogenetic characteristics of TFE3 translocation RCC. Methods and Materials: The clinical data of a 52-year-old-female patient with TFE3 translocation RCC exhibiting rare morphological characteristics was analyzed, and the tumor tissues were probed using histopathological staining, immunohistochemistry, and fluorescence in situ hybridization (FISH). In addition, the relevant literature was reviewed. Results: This case is a TFE3 translocation RCC with rare morphological features. It composed of two types of tumor cells. TFE3 and pax-8 were diffusely and strongly expressed in both tumor cells, and they were partially positive for CAIX, RCC, CK, EMA, CD10, Vim, Melan-A, and p504s. Only 2% of the cells were positive for the proliferation marker Ki-67, and the tumor was negative for CK7, CD117, Inhibin-α, HBM45, and p53. FISH showed a positive signal for TFE3 translocation. Conclusions: This case was a TFE3 translocation RCC with rare morphological features. Through this case report, we emphasize the importance of in situ detection of TFE3 gene translocation and protein in TFE3 translocation RCC.

Keywords: FISH, pathological feature, renal cell carcinoma, TFE3 translocation RCC

How to cite this article:
Xia T, Long H, Liao D, Wang W, Xiao X. A case of TFE3 translocation renal cell carcinoma with rare morphological features and literature review. Indian J Pathol Microbiol 2023;66:135-40

How to cite this URL:
Xia T, Long H, Liao D, Wang W, Xiao X. A case of TFE3 translocation renal cell carcinoma with rare morphological features and literature review. Indian J Pathol Microbiol [serial online] 2023 [cited 2023 Feb 7];66:135-40. Available from: https://www.ijpmonline.org/text.asp?2023/66/1/135/367981





   Introduction Top


TFE3 translocation renal cell carcinoma (RCC) is a rare type of kidney tumor and it accounts for approximately 1% of RCC.[1] This disease is characterized by a gene fusion resulting from the translocation of TFE3 on chromosome Xp11.2 to another chromosome. These chimeric gene fusions result in overexpression of the TFE3 fusion protein. It is a malignant tumor of the kidney with an advanced stage and a poorer prognosis than conventional clear cell RCC in older adults.[2] TFE3 translocation RCC accounts for 20 ~40% of pediatric RCCs and only 1.6 ~4% of adult RCCs, in addition, pediatric TFE3 translocation RCC has a better prognosis compared with its adult counterpart.[3]

In this report, we present a case of TFE3 translocation RCC with rare morphological features and discuss the uncommon features of this case as determined by histopathological, immunohistochemical, and molecular approaches.


   Subjects and Methods Top


Specimens

The paraffin-embedded tissue samples of TFE3 translocation RCC patients were obtained from the Department of Pathology, the Affiliated Hospital of Southwest Medical University in April 2018. The patient was a resident of Sichuan, Lu Zhou. The clinico-pathological information of the patient, including age, tumor size, tumor location, gender, operation method and prognosis, were also obtained. The experimental protocol was pre-approved by the Medical Ethics Committee of Southwest Medical University (No. 20130051).

Immunohistochemistry

Biopsy specimens were fixed with 10% formaldehyde, dehydrated, embedded in paraffin, and cut into 4 μm-thick sections. For general histopathological examination, the sections were stained with hematoxylin and eosin, and observed under a light microscope. Immunohistochemical staining uses the Evasion two-step method. Antibodies used in the experiment include PAX8, RCC maker (RCC, 66.4.C2, ZSGB-BIO Co., Ltd, Bei Jing, China), Cytokeratin (CK, AE1/AE3, Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China), Epithelial membrane protein (EMA, E29, 1:100, Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China), cluster differentiation (CD10, 56C6, Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China), Carbonic Anhydrase IX (CA9, H-11, ZSGB-BIO Co., Ltd, Bei Jing, China), Alpha-MethylacylCoA Race (AMACR; P504S, 13H4, 1: 100, Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China), Melan A (A103, ZSGB-BIO Co., Ltd, Bei Jing, China) and negative for cytokeratin 7(CK7, MX053, Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China), Melanosome (HMB45, ZSGB-BIO Co., Ltd, Bei Jing, China), and CD117, Inhibin-alpha, p53(Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China, 1:100), ki-67(Fuzhou Maixin Biotechnology Co., Ltd, Fuzhou, China, 1:100). A sample was considered positive for any of the above markers if ≥1% of the tumor cells stained positive.

In situ hybridization

Fluorescence in situ hybridiyation (FISH) was performed by Guangzhou Da 'An Technology Co. Ltd. Due to the involvement of the X chromosome, TFE3 translocation in female samples was inferred by the presence of red, green, and fusion (yellow) signals, and by red and green signals in the male samples. Two fused signals in females and one fused signal in males indicated a negative result. For each sample, 100 cells were counted and only non-overlapping nuclei were included. As per the threshold of most commercial probes, the result was considered positive when the isolated signal appeared in >10% of the tumor cells.


   Results Top


Patient and clinical history

A 52-year-old woman was introduced to the affiliated hospital of southwest medical university from a private hospital for “low back pain for half a year and aggravation for 3 months.” Half a year ago, she felt low back pain for unknown reasons and a cyst occupied her right renal area detected by abdominal ultrasound examination [Figure 1]a. She did not receive any treatment as her symptoms relieved. Three months ago, the low back pain symptoms were significantly aggravated, without hematuria. Abdominal CT scan revealed a right renal tumor, 4 cm in diameter, showing poor blood supply and well-defined margins [Figure 1]b. She did not have any family history or other medical history. The patient underwent radical resection of right renal carcinoma and renal hilar lymph node dissection in April 2018 under general anesthesia.
Figure 1: (a) Abdominal ultrasonographic examination: enhanced heterogeneous echo of the right kidney, 4 × 3.6 cm. (b) Abdominal CT scan: right kidney mass, round, measured 4 × 3.5 cm (arrow).(c) the mass was located in the middle pole of the kidney (arrow), measured 4cm × 3.5cm × 2.5 cm. The tumor was polycystic, with thin and soft cyst wall and clear boundary

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Pathological examination

Visual examination

On examination, an intact kidney with perinephric fat measuring 10 × 7 × 5 cm and weight of 935 g was seen. The tumor was located in the middle pole of the right kidney. It was a well-circumscribed pale polycystic mass, limited to the kidney, without hemorrhage and necrosis, sized 4 cm × 3.5 cm × 2.5 cm. It had a thin and flat cyst wall containing the yellowish fluid inside [Figure 1]c.

Microscopic examination

The tumor showed polycystic characteristics [Figure 2]a, the lining epithelium admixed with two types of neoplastic cells, and formed a nest and glandular architecture. Besides nest and glandular structures, the epithelial lining also showed multilayering, tufting as well as branching papillary structures. One type of neoplastic cells with clear cytoplasm formed nests in tumor stroma [Figure 2]b. Another type of neoplastic cells with eosinophilic cytoplasm, shaped like a nail, formed glandular structure in the tumor stroma [Figure 2]c. The two types of lining epithelium showed mild to morderate cytologic atypia. The psammoma bodies were seen. The nucleoli are conspicuous at ×400 magnifcation and visible, so the nuclear Grade was 2 and corresponded to ISUP/WHO; the pathological stage of tumor was pT1a N0 M0 with negative surgical margin. At present, the patient recovered well after surgery without recurrence and metastasis.
Figure 2: (a) The tumor area was polycystic with thin cyst wall and bleeding inside the cyst, 100 × HE. (b) The cytoplasm of some tumor cells is abundant, with light staining to clear and well-defined, and is attached to the inner wall of the cyst or cystic wall stroma to form transparent tumor cell nests, 200 × HE. (c) The cytoplasm of some tumor cells is rich in eosinophilic granules, which are attached to the inner wall of the capsule to form boot-like structures, or form glandular cavity-like structures in the tumor stroma, 200 × HE

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Immuno-phenotyping

Both types of tumor cells showed high intensity and diffused nuclear staining of TFE3 [Figure 3]a, and were positive for pax-8, CAIX, RCC, CK, EMA and CD10. Weak staining was observed for Vim, Melan-A, and p504s, and the tumor cells were negative for Ki-67, CK7, CD117, Inhibin-α, HBM45, and p53.
Figure 3: (a) The immunohistochemistry of tumor: Strong positive expression of TFE3 in both tumor cells' nucleus, 200 × Evasion two-step method. (b) FISH showed TFE3 gene breakage and translocation in 73% of the tumor cells

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In situ detection of TFE3 gene translocation and protein

FISH showed TFE3 gene breakage and translocation in 73% of the tumor cells [Figure 3]b.


   Discussion Top


TFE3 translocation RCC is a rare form of RCC that was first described in 1995 by Dijkhuizen et al.[4] In 2004, it was first listed as a separate subtype of kidney cancer by the World Health Organization. Now, it is included in MiT family translocation RCC according to the 2016 WHO renal tumor classifcation.[5] This type of RCC often occurs in children and adolescents, compared with adult patients, It accounts for 40% of renal cell carcinoma in children and only 1.6 ~4% of renal cell carcinoma in adults. Adult patients with TFE3 RCCs are often diagnosed in an advanced stage with more aggressive and poor prognosis.[6] Argani et al.[7] reported that the majority of patients with this RCC subtype are females, with male to female ratio of 6:22. We reviewed 89 cases (aged 3–70 years) of TFE3 translocation RCC that have been documented in China since 2007, of which 53 were females and 36 were males [Table 1].[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36] The clinical presentation of TFE3 type RCC is similar to that of conventional clear cell RCC or papillary RCC; so the frequency of TFE3 RCCs in adults may be underestimated.[37] In our case, the female patient was an adult with initial symptoms such as back pain and the presence of an occupying mass in the kidney. These symptoms are consistent with previous reports in the literature.
Table 1: 89 cases of clinical features of TFE3 RCCs in China

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Pathological examination

Visual inspection

TFE3 RCCs do not have a distinctive gross appearance, most of its gross features are similar to those of conventional clear cell RCC.[38] The cystic cut surfaces of the tumor are usually caused by hemorrhage and necrosis. The tumor differs in terms of size and distribution. Among the 89 cases reviewed, 20 cases occurred in the left kidney and 23 cases in the right kidney. The diameter of the tumors ranged from 4 to 7 cm.[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36]

Microscopic examination

Most distinctive histological pattern of the Xp11 translocation RCCs is that of a papillary, alveolar, and nested neoplasm composed of clear and eosinophilic cells with abundant psammoma bodies.[39] TFE3 RCCs are usually composed of papillary and solid cardiopulmonary vacuoles. Tumor cells are arranged in pseudostratification with abundant clear to eosinophilic cytoplasm and high grade nuclei There are sand granules and melanin in the tumor, and the morphology is similar to the pigmented perivascular epithelioid tumor (PEComa). However, some scholars believe that less sand corpuscles and transparent spheres, as well as more nested structures may lead to the diagnosis of Xp11.2-translocated RCC fusion with ASPL-TFE3.[40] In our case, the tumor showed polycystic characteristics in both gross and histological appearance, which are not caused by hemorrhage and necrosis. Morphologically, it lacks the features of papillary neoplasm composed of clear and eosinophilic cells, abundant psammoma bodies, and nuclear grade corresponded to ISUP/WHO Grade 2. These characteristics are rarely reported in previous literature.

Immunohistochemistry and molecular subtypes

Like most RCCs, TFE3 RCCs express PAX8 and other renal tubular marker, but underexpress epithelial markers such as cytokeratins and epithelial membrane antigen, often express the cysteine protease cathepsin K, and may express melanocytic markers. Strong and diffuse nuclear TFE3 immunoreactivity using an antibody to the C-terminal portion of TFE3 is highly sensitive and specific for the TFE3 translocation RCC,[41] and TFE3 break-apart FISH assay is more useful for diagnosis.[42],[43] Among the 70 cases we reviewed, tumor cells in 100% cases were TFE3 immunoreactive; only 13 cases have taken the FISH assay [Table 2]. In our case, tumor cells' nucleus showed strong diffuse staining for TFE3. Our next step was to detect the type of fusion gene.
Table 2: 70 cases of pathological features of TFE3 RCCs in China

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In 2013, the Xp11.2 translocation RCCs and t (6;11) RCCs are classified as a member of MiT family translocation RCCs by International Society of Urologic Pathology Vancouver. Until 2016, it was recorded by the WHO as a subtype of RCC.[44] The mutant subtypes of MITF/TFE family RCCs include MITF, TFE3, TFEB, and TFEC, which share homologous DNA binding and activation domains. According to the reports of Argani et al.,[45] there were five TFE3 fusion gene types of Xp11.2-RCC reported, including ASPL-TFE3, PRC-TFE33, PSF-TFE3, CLTC-TFE3, and non-TFE3. Among them, the most common Xp11.2-translocated RCC subtypes were ASPL-TFE3, and PRC-TFE33. Currently, more new fusion genes generated by the translocation of Xp11.2 chromosome in this tumor has been found, which include RBM10-TFE3, MED15-TFE3, MATR3-TFE3, and FUBP1-TFE3.[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36]

Differential diagnosis

The differential diagnosis of TFE3 RCCs includes: (1) Clear cell papillary RCC: the neoplasm is composed of clear cells with low-grade nuclei, no eosinophilic cytoplasm, no calcifications, and usually branched ductal structures with nuclei lining secretory cells above the basement membrane CK7+, CAIX expression follows a cup-shape pattern, CD10 -, AMACR -, TFE3 -. (2) Clear cell renal cell carcinoma: older patients, no true papillae, lack the nested and alveolar growth pattern.[46] Frequently positive with keratin/EMA, vimentin, diffuse CAIX in a box-shape pattern, 3p deletion present and TFE3-, for our case, it should be differentiated from cystic degeneration of clear cell RCC. (3) Clear cell sarcoma of kidney: patients are usually children, cells have indistinct cell borders, TFE3-. (4) Papillary RCC: the neoplasm has more prominent papillary structures, no nested alveolar patterns, no extensive areas of clear cells; CK7+, AMACR+, TFE3-. (5) Epithelioid angiomyolipoma: The tumor composed of smooth muscle, adipose tissue and vasculature. The neoplastic cells may have an epithelioid morphology, nuclei may also appear as low- to mild-grade nuclei, and may even be giant cells of odd-looking multinucleoma. It usually has more mitotic figures, and expresses HMB45, melan A, cathepsin K, and smooth muscle expresses actin and muscle-specific actin. Some tumors may show TFE3 immunoexpression, but the immunoreactivity is often weak. (6) Low-grade potential multilocular cystic renal cell tumor: Thin fibrous septae with clear cells lining the septa or in small clusters. Low-grade nuclei without nucleoli (ISUP grade 1-2). Cyst lining may be denuded and bland clear cells in septa may be mistaken for lymphocytes; look of vascularity. No expansile growth of clear tumor cells or showed solid nodules. No necrosis, vascular invasion or sarcomatoid change. Immunohistochemistry shows that the tumor cells are strongly positive for PAX8 and CAIX, AMACR negative in most cases.

Treatment and prognosis

The first choice for the treatment of TFE3 RCCs include radical nephrectomy, and renal hilar lymph node dissection should be performed at the same time if the patients have lymph node metastases. Malouf et al.[47] suggests that vascular endothelial growth factor receptor (VEGFR-) targeting agents and/or mammalian rapamycin (mTOR) targeting inhibitors may be beneficial in patients with TFE3 RCCs. Selective MET inhibitors appear to have modest antitumural activity. Altinok et al.[1] reported that the postoperative survival time was correlated with reno-vascular infiltration, and tumor size. Among 89 cases we reviewed, five cases had renal hilar lymph node metastasis, four cases had intravascular tumor thrombosis and three cases had bone metastasis, with follow-up time ranging from 4 to 19 months.[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36] Currently, due to the small number of cases of TFE3 RCCs reported in the literature, there is no unified treatment, and its biological behavior and patient prognosis are still uncertain. Increased awareness of this disease among urologists, pathologists, and oncologists is necessary in order to help in identifying more cases of this phenotype in the future. In our case, the patient received sorafenib after the surgery. There is a no evidence of recurrence found since the operation.

In conclusion, we present a case with rare morphological features that may be diagnosed as TFE3 translocated RCC. Its histological morphology, immunohistochemistry, and molecular findings are characteristic of TFE3 RCCs rather than other renal tumors.

Acknowledgment

There are no conflicts of interest.

Financial support and sponsorship

This study was partly supported by operating research grants from Southwest Medical University School-level Project (Youth Fund), NO. 2017-ZRQN-126.

Conflicts of interest

There are no conflicts of interest.



 
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Correspondence Address:
Xiuli Xiao
Department of Pathology, The Affiliated Hospital of Southwest Medical University, Luzhou - 646 000
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijpm.ijpm_755_21

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