 Abstract | | |
Follicular dendritic cell sarcoma (FDCS) is a rare tumor, which mainly originates from follicular dendritic cells (FDCs) in the lymph nodes. Sometimes FDCS can arise from outside the lymph nodes. FDCS is an extremely rare malignant tumor in intraperitoneal or retroperitoneal tissue. We gathered the detailed clinical data of three patients diagnosed with FDCS in the abdomen. The clinical observations and histopathologic and immunohistochemical features of FDCS were analyzed. The patients included two men and one woman aged 55 ~ 61 years old. The mesentery of the small intestine and colon was involved in case 1, spleen in case 2, and retroperitoneal tissues in case 3. Two patients presented with abdominal masses, and one presented with no obvious symptoms. Histology showed ovoid to spindle neoplastic cells arranged in fascicles and storiforms with inflammatory infiltrate as well as whorled patterns in some areas. Immunohistochemical staining was positive for CD21, CD23, CD35, and SSTR2. FDCS exhibits no characteristic clinical manifestations. Morphologically, FDCS can have overlapping features with many other entities, leading to misdiagnosis. The use of histopathology supplemented with FDC markers, such as CD21, CD23, and CD35, is useful for diagnosis and differential diagnosis.
Keywords: Abdominal cavity, diagnosis, extranode, follicular dendritic cell sarcoma, immunohistochemistry
How to cite this URL:
Yan J, Wu Q, Hu Y, Nai T. Clinicopathologic profile of intra-abdominal follicular dendritic cell sarcoma: A study of three cases with a literature review. Indian J Pathol Microbiol [Epub ahead of print] [cited 2023 Jun 10]. Available from: https://www.ijpmonline.org/preprintarticle.asp?id=368568 |
| Introduction | |  |
Follicular dendritic cell sarcoma (FDCS) is a rare malignant tumor with histopathologic and immunophenotypic characteristics similar to those of follicular dendritic cells (FDCs). The disease entity was first described in 1986 by Monda et al.[1] Since then, FDCS has been reported increasingly. However, the incidence of FDCS is low, and fewer than 400 cases have been reported in the English literature. Large-scale research data on clinical, histological, and prognostic parameters are lacking. The World Health Organization classification of hematopoietic and lymphoid tissue tumor classifies this entity as a histiocytic and dendritic cell neoplasm. FDCS generally occurs in lymph nodes—most commonly, the cervical, mediastinal, or axillary lymph nodes. In approximately one-third of cases, FDCS can also be found in extranodal sites.[2] In recent years, the incidence of FDCS occurring outside the lymph nodes has been increasing. The diagnosis of FDCS, particularly extranodal FDCS, presents a challenge for pathologists. Increasing awareness about the existence of FDCS at extranodal sites may aid in the reduction of diagnostic errors. The study presents three cases of intra-abdominal FDCS based on clinical features and histomorphology and immunophenotypes and reviews the literature.
| Case Report | | |
Case 1
A 61-year-old female patient visited the hospital presenting with a pelvic neoplasm with dull pain in the lower abdomen in February 2019. Physical examination revealed a mass lesion 10 cm in diameter near the uterus. Ultrasound examination confirmed the presence of a pelvic mass. Contrast-enhanced computed tomography (CECT) of the abdomen revealed a nodular cystic-solid mass in the right lower abdomen and pelvic cavity with a size of 9.8 cm × 5.2 cm and enhancement. In addition, multiple nodular soft tissue density shadows were noted, and the largest shadow was located near the cecum with a diameter of approximately 4.3 cm. It was considered a right lower abdomen-pelvic neoplasm with surrounding implant metastases and suspicious liver metastases [Figure 1]a. The clinician considered the high possibility of malignant tumors (unclear boundary with the small intestine). The patient was suggested to undergo surgery to resect the mass and then received exploratory laparotomy and lesion resection in the hospital. The patient denied radiotherapy and chemotherapy, and the patient died approximately 1 year after the operation. | Figure 1: (a) CECT of the abdomen revealed a nodular cystic-solid mass in the right lower abdomen and pelvic cavity; (b) CECT showed an inhomogeneous enhanced nodule of the spleen; (c) CTA revealed that the larger nodule was located on the right side of the abdominal cavity
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Case 2
A 61-year-old male patient was admitted to the hospital in April 2021 due to a space-occupying lesion of the spleen found by physical examination for more than 6 months. The patient had no obvious positive symptoms or signs. Computed tomography (CT) of the abdomen revealed splenic space-occupying lesions measuring 4.6 × 5.1 cm. CECT showed an inhomogeneous enhanced nodule of the spleen, inhomogeneous enhancement at the edge of the lesion, and low density in the center that was not enhanced [Figure 1]b. The patient then underwent laparoscopic total splenectomy in the hospital and recovered without additional treatment. The patient was free of disease at 5 months of follow-up.
Case 3
A 55-year-old male patient visited the doctor in May 2021 presenting with an abdominal mass found for 2 months and fever for 1 week. Physical examination revealed a large mass 20 cm × 20 cm in size in the right abdomen, and the body temperature was 38.4°C. Abdominal aorta CT angiography (CTA) showed multiple mass soft tissue density shadow in the abdominal cavity. The larger mass measuring 19.5 cm × 12.8 cm was located on the right side of the abdominal cavity with an unclear boundary. The enhanced scan showed obvious early enhancement, but the low density shadow was not enhanced. The smaller focus was located in the pelvic cavity and was approximately 8 cm × 6.2 cm in size, and the enhanced scan was obviously enhanced and more uniform. In addition, multiple nodular soft tissue density shadows were observed in the right omentum. Multiple masses in the abdominal cavity with invasion of the right colon and omentum were considered. The blood supply of the larger focus came from the superior mesenteric artery, and the blood vessel of the pelvic focus originated from the duodenal artery [Figure 1]c. The patient underwent exploratory laparotomy and complete excision of the lesions. The patient continued to receive four cycles of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) after the operation. The patient was generally in good condition at the 4-month follow-up.
| Materials and Methods | | |
Tissue specimens were collected for 10% buffered formalin fixation, grossing, routine dehydration, embedding into paraffin, and sectioning into 4μ-m-thick sections for hematoxylin and eosin staining. Immunohistochemistry was performed with EnVision two-step staining, EBER in situ hybridization and light microscope reading. Antibodies against CD21, CD23, CD35, SSTR2, ALK, CD30, CD20, CD3, CD117, DOG-1, CD34, EMA, PCK, SMA, desmin, D2-40, CXCL-13, Ki-67, S-100, vimentin, IgG4, and IgG were purchased from Shanghai Roche.
| Results | | |
Macroscopic features
Three cases underwent excision of the lesions. Among them, multiple masses were found in two cases (cases 1 and 3). One case involved the mesentery of the small intestine and colon and the abdominal wall of the uterus and pelvic wall, and the other involved retroperitoneal tissues. Tumors could also be seen in the omentum and mesentery of the small intestine in case 3. The spleen was involved in case 2. In all the cases, the tumors were well circumscribed. The cut surfaces were nodular and fleshy [Figure 2]. In case 3, one of multiple masses was partly projected into the gut lumen and infiltrated into the wall, and the tumors exhibited marked heterogeneity, showing fleshy areas along with areas of hemorrhage and cystic changes. The other two cases showed a homogeneous fleshy appearance. | Figure 2: Gross features of three cases of FDCS. (a) Several gray-red nodules are noted in the small intestine and colonic mesentery, the largest of which is 12 cm × 9 cm × 8.5 cm; (b) A gray-white nodular mass of 5.5 cm x 4.8 cm x 4.5 cm was observed in the spleen; (c) The larger tumor was located on the serous surface of the intestinal canal, which was nodular in shape and 20 cm x 19 cm x 16 cm in size. Multiple gray-white and gray-red nodules were observed in the omental tissue
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Histomorphology
Of the three cases, two cases were conventional FDCS, and the other one was inflammatory pseudotumor-like FDCS. Two conventional FDCS cases exhibited similar histomorphological features. The tumors all showed biphasic cytological morphology, which was composed of oval to spindle neoplastic cells. The neoplastic cells were arranged in fascicular somewhat syncytial sheets with whorled or storiform patterns noted in some areas. Individual tumor cells showed oval, round, or fusiform nuclei with vesicular chromatin, smooth nuclear membranes, nuclear pseudoinclusions, and indistinct to prominent small nucleoli. Focal nuclear atypia with scattered bi- or multinucleated cells was also noted [Figure 3]. Mitosis were observed. Numerous small mature lymphocytes were noted throughout the tumors. One case showed small areas of necrosis (case 3). Inflammatory pseudotumor-like FDCS featured a rich lymphoplasmacytic infiltrate accompanied by a few scattered reactive lymphoid follicles, and tumor cells exhibited a scattered appearance. Spindled to oval neoplastic cells with poorly defined cell borders were dispersed or formed loose whorled fascicles in an inflammatory background. These cells possessed medium amounts of eosinophilic cytoplasm and vesicular nuclei with stippled chromatin and small but distinct nucleoli. Local necrosis was found in case 2, and granulomatous inflammation was observed around the necrotic focus.
Immunohistochemistry
CD21, CD23, and CD35 were expressed in two cases of conventional FDCS [Figure 4]. Diffuse positive expression of SSTR2, D2-40, CXCL-13, and vimentin was detected, whereas CD117, CD34, DOG-1, S-100, desmin, SMA, CD30, ALK, EMA, and PCK were not expressed. The infiltrating lymphocytes between tumor cells comprised a mixture of CD20-positive B cells and CD3-positive T cells. The Ki-67 index was approximately 30 and 70% (cases 1 and 3), respectively. Inflammatory pseudotumor-like FDCs in the spleen expressed CD21, CD23, and CD35 to varying degrees [Figure 5]. SSTR2 and SMA were diffusely positive, but D2-40, CXCL-13, vimentin, ALK, and CD34 were negative. The IgG4 to IgG ratio was approximately 70%, positive cells >100/HPF, and the Ki-67 index was approximately 10%. The background included a mixture of CD20+ B cells, CD3+ T cells, tissue cells, and plasma cells. | Figure 4: Conventional FDCS. (a) The tumor cells were oval to spindle neoplastic cells that were arranged in fascicles or patches, and numerous lymphocytes were present among the tumor cells. (HE, X100); (b-d) Neoplastic cells are immunoreactive for CD21, CD35, and CD23. (SP, X40)
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 | Figure 5: Inflammatory pseudotumor-like FDCS. (a) The tumor background includes a large number of plasma cells, lymphocytes, and histiocytes scattered throughout the tumor with some tumor cells. Spindled to oval neoplastic cells with poorly defined cell borders were dispersed or formed loose whorled fascicles. A mitotic image can be observed. (HE, X400); (b-d) Immunohistochemical staining showed different degrees of CD21, CD35, and CD23 expression (SP, X200)
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In situ hybridization
In situ hybridization for EBER highlighted the nuclei of the tumor cells in case 2, whereas EBER was negative in two cases of conventional FDCS [Figure 6]. | Figure 6: (a) EBER was negative in two cases of conventional FDCS. (b) In situ hybridization for EBER highlighted the nuclei of the tumor cells in case 2 (EBER, X100)
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| Discussion | | |
FDCS is an uncommon malignant tumor that originates from the follicular germinal center of lymph nodes or FDCs in extranodal lymphoid tissue. FDCs are stromal-derived immune accessory cells that play an important role in antigen presentation. Therefore, FDCS can occur in lymph nodes or a wide variety of extranodal sites. In 1997, Chan et al.[3] published extranodal FDCS for the first time. Extranodal sites can involve almost all organs of the body, including the head and neck, retroperitoneum, mesentery, spleen, gastrointestinal tract, liver, soft tissue, lung, pancreas, skin, and breast, but intra-abdominal locations are very rare. FDCS can occur in all age groups but shows adult predominance with a mean age of approximately 44 years. It presents with almost equal frequency in both genders.[4] The clinical manifestations vary according to the location of the disease, but it often presents as a slow growing mass. Lesions that occur in the intra-abdominal location may be associated with systemic symptoms, such as abdominal pain or fatigue, fever, and night sweats. The male to female ratio of three patients with FDCS was 2:1, and the age of onset was 55 to 61 years. Two of the patients all manifested abdominal masses, of which one mostly involved the mesentery of the small intestine and colon and suspected liver metastasis, and the other mainly involved retroperitoneal tissues. Case 1 experienced dull pain in the lower abdomen, and case 3 had a fever. Inflammatory pseudotumor-like FDCS occurred in the spleen. The patient had no obvious symptoms or signs. The tumor was found by physical examination.
The etiology and pathogenesis of FDCS are not entirely clear and may be related to Castleman disease, EBV infection, and autoimmune diseases. Some studies suggest that FDCS may evolve from hyaline vascular Castleman disease possibly through a mechanism involving epidermal growth factor receptor (EGFR).[5],[6] Therefore, Castleman's disease may be the precursor of FDCS. Some patients are complicated with skin paraneoplastic pemphigus, systemic lupus erythematosus, and other diseases, so some scholars think that FDCS may be related to immune system diseases.[7] Inflammatory pseudotumor-like FDCS in the liver and spleen is typically associated with EBV infection, whereas only 4% of conventional FDCS is associated with EBV infection.[8] In this group, two cases of conventional FDCS were negative for EBER in situ hybridization, whereas inflammatory pseudotumor-like FDCS in the spleen was EBV positive, which was consistent with the literature report. In recent years, it has been reported that some cases of FDCS are accompanied by an increase in IgG4-positive plasma cells. A study of 114 cases of IgG4-related diseases by Zen and Nakanuma showed that the plasma cell IgG4/IgG of most patients with IgG4-related diseases was greater than 30%. However, in cases of nonIgG4-related diseases, IgG4/IgG was less than 10%.[9] Takeuchi et al.[10] showed that the number of EBV-infected cells increased in IgG4-related lymphadenopathy, indicating that a relationship may exist between IgG4-related diseases and EBV. In six cases of EBV-positive splenic inflammatory pseudotumor-like FDCS reported by Choe et al.,[11] the ratio of IgG4-positive plasma cells to HPF and IgG4/IgG was 25%–75%, suggesting that EBV plays a key role in inflammatory pseudotumor-like FDCS and IgG4-related sclerosing diseases. In this group, one patient with EBV-positive inflammatory pseudotumor-like FDCS in the spleen showed a large amount of plasma cell infiltration in the tumor tissue. Immunohistochemistry showed that the plasma cell IgG4:IgG ratio was approximately 70%, and the rate of positive cells was greater than 100/HPF, which was consistent with the literature report.
FDCS lacks specific clinical and imaging findings, and the diagnosis depends on pathological examination. The density or signal intensity of 3 FDCS tumors was inhomogeneous on plain scan, and all tumors showed inhomogeneous enhanced nodules on enhanced CT. Generally, FDCS is a relatively well-defined solid mass with a diameter of 1–20 cm. The section is gray–white, grayish red, and solid, with hemorrhage, necrosis, or cystic degeneration. If it occurs in the abdominal cavity, the volume of the tumor is generally large and often accompanied by bleeding and necrosis. In case 3, the maximum diameter of the tumor was 20 cm, and necrosis could be observed, which may be related to the large volume of the tumor and insufficient blood supply. FDCS exhibits variable morphologic features. Most exhibit a spindle cell morphology showing interlacing fascicles, a storiform pattern, and whorls of spindled tumor cells, whereas others reveal syncytial sheets of epithelioid tumor cells. The tumor cells exhibit indistinct cytoplasmic borders, fine nuclear chromatin with clearly outlined fine nuclear membranes, and small but distinct nucleoli. Mitoses are scarce. Some tumors may show multinucleate tumor cells or cells with multilobate nuclei. Groups of small mature lymphocytes are found throughout the tumors. Inflammatory pseudotumor-like FDC sarcoma, which is also known as inflammatory pseudotumor-like follicular/fibroblastic dendritic cell sarcoma, is a distinctive type of FDC sarcoma clinically and pathologically different from conventional FDC sarcoma, featuring inflammatory pseudotumor-like histology and consistent association with EBV. Inflammatory pseudotumor-like FDC sarcoma occurs predominantly in the liver and spleen with a marked female predilection. The histological characteristics of three cases of FDCS in this group were very consistent with those of FDCS described in various published studies. Immunohistochemical staining plays an important role in diagnosis. FDCS often shows one or more FDC markers, such as CD21, CD35, and CD23. Among them, CD21 and CD35 are highly sensitive and specific. Other markers commonly expressed include Clusterin, Fascin, CXCL13, D2-40, EGFR, SSTR2, FDCSP, and SRGN,[12],[13] which can improve the accuracy of FDCS diagnosis when combined with CD21, CD23, and CD35. S100 protein, EMA, and CD68 are variably expressed. FDCS is usually negative for cytokeratins, CD1α, CD3, CD79a, CD34, and MPO. Immunohistochemical staining showed that CD21, CD23, CD35, SSTR2, D2-40, CXCL-13, and vimentin were diffusely expressed in two cases of conventional FDCS. Inflammatory pseudotumor-like FDCs that occurred in the spleen showed varying degrees of expression of CD21, CD23 and CD35, and SSTR2, SMA was diffusely positive, but D2-40, CXCL-13, and vimentin were negative. Of note, inflammatory pseudotumor-like FDCs do not reliably express CD21, CD23, or CD35 but always exhibit an EBV association.
Due to the limited number of reported cases and similar histomorphological features to some other tumors, a proportion of FDCSs, particularly extranodal FDCSs, are difficult to recognize and easy to misdiagnose. Most tumors in the retroperitoneum and colon were believed to be gastrointestinal stromal tumors (GISTs) on morphology. FDCS that occurs intraperitoneally or retroperitoneally should be differentiated from GIST, lymphoma, inflammatory myofibroblastic tumor, interdigitating dendritic cell sarcoma, etc. GISTs are composed of spindle cells and/or epithelioid cells with consistent morphology. Positive expression of CD117, CD34, and DOG-1 is helpful for differentiation. The diffuse distribution of FDCS tumor cells is easily confused with lymphoma. Nuclear pleomorphic tumor cells are similar to diffuse large Bcell lymphoma or anaplastic large cell lymphoma. These conditions can be distinguished by CD30, T cell, B cell-related markers, and FDC markers. The morphology of interdigitating dendritic cell sarcoma was similar to that of FDCS, but it was difficult to differentiate morphologically. Immunohistochemically, S-100, vimentin, and CD45 were expressed, but no FDC markers were expressed. Although Langerhans cell sarcoma cells are atypical, they still exhibit the characteristics of Langerhans cells. The nucleus of the tumor is kidney-shaped or horseshoe-shaped, folded and twisted, and a nuclear sulcus can be observed. Tumors express CD1α, S-100, and Langerhans but do not express FDC markers. Inflammatory myofibroblasts are mainly composed of myofibroblasts and fibroblasts with a large amount of inflammatory cell infiltration in the stroma. SMA, desmin, and ALK are expressed by immunohistochemical staining, but no FDC markers are expressed. Inflammatory pseudotumors, having excluded inflammatory myofibroblastic tumors, are nonneoplastic lesions that are probably inflammatory or reparative in nature and closely mimic EBV+ inflammatory FDC sarcoma except that spindly cells lack nuclear atypia, FDC markers, and EBV. In addition, the morphologic differential diagnoses also include sarcomatoid carcinoma, thymoma, schwannoma, ectopic meningioma, and metastatic melanomas.
With the deepening of the understanding of the disease, most scholars think that FDCS is at least a sarcoma of intermediate grade. The disease has the potential for local recurrence (40% to 50%) and systemic metastasis (20% to 25%), and 10% to 20% of patients eventually die of the disease. Metastases to the lung, liver, or lymph nodes have been noted through the blood and lymphatic system. In this group, two patients with conventional FDCS had large tumors, and multiple metastases were found, suggesting that the tumor was highly invasive. In contrast, the biological behavior of inflammatory pseudotumor-like FDCS was relatively inert, which was consistent with most of the literature reports.
At present, there is no consensus on the treatment of FDCS. Complete surgical resection is the best treatment, and its prognosis is related to the patient's age, tumor location, size, cell atypia, mitosis, necrosis, and metastasis. FDCS is characterized by significant cytological atypia, extensive coagulative necrosis, high proliferation index, tumor diameter >6 cm, and poor prognosis of patients located in the abdomen.[4] Surgical resection is the first choice for localized lesions, and radiotherapy and/or chemotherapy can be used for patients with large tumors, deep tumors that are not easily resectable, or tumors that cannot be operated on as well as cases of recurrence and metastasis. To date, studies have shown that surgery alone is still associated with a high local recurrence rate, whereas the choice of radiotherapy and chemotherapy is also controversial.[14] All three patients in this group were treated with surgical resection. Case 3 received four cycles of CHOP after the operation, whereas the other two patients did not receive chemotherapy or radiotherapy. Case 1 died approximately 1 year after the operation. The other two patients were followed up for 4 months and 5 months, separately, and the patients survived. No signs of local recurrence or distant metastasis were noted.
In summary, as a rare malignant tumor, the incidence of FDCS is low, and its histomorphology is similar to that of many other tumors. Therefore, it is necessary to improve the understanding of the disease and maintain a high degree of vigilance. FDCS should be considered, especially in the differential diagnosis of extranodal spindle cell tumors, to avoid misdiagnosis. Immunostaining for FDC markers in such a situation may properly reveal the disease.
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Conflicts of interest
There are no conflicts of interest.
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Correspondence Address:
Yuchang Hu,
Department of Pathology, Yichang Central People's Hospital, No. 183 Yiling Road, Yichang - 443 003
China
 Source of Support: None, Conflict of Interest: None DOI: 10.4103/ijpm.ijpm_1089_21
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6] |
