Intraabdominal follicular dendritic cell sarcoma: a report of three cases and review of the literature
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1 Tu mo ri, 99: e65-e69, 2013 Intraabdominal follicular dendritic cell sarcoma: a report of three cases and review of the literature Yuksel Urun 1, Duygu Kankaya 2, Lokman Koral 3, Bulent Yalcin 4, Ayca Karabork 2, Koray Ceyhan 2, Melih Cem Boruban 3, Gungor Utkan 1, and Ahmet Demirkazik 1 1 Department of Medical Oncology, and 2 Department of Medical Pathology, Ankara University Faculty of Medicine, Ankara; 3 Department of Medical Oncology, Selcuk University Meram Faculty of Medicine, Konya; 4 Department of Medical Oncology, Yildirim Beyazit University Faculty of Medicine, Atatürk Research and Educational Hospital, Ankara, Turkey ABSTRACT Follicular dendritic cell sarcoma (FDCS) is a rare neoplasm that originates from follicular dendritic cells in lymphoid follicles. FDCS has been increasingly reported in recent years. However, data on FDCS are mostly based on single case reports or case series and its natural history and standard treatment are not clear. To increase the understanding of this rare disease, we report our experience of three cases of FDCS with an analysis of the morphological and immunophenotypic characteristics, clinical course, treatment options and response to treatment. In addition, we reviewed the literature on FDCS. Introduction Dendritic cell neoplasms (DCNs) are rare tumors that affect the lymphatic system. Since their first description by Monda et al. 1 in 1986, there has been increased reporting of DCN in recent years. Normal dendritic cells are a heterogeneous group of nonlymphoid cells. Four types of dendritic cells exist: follicular, interdigitating, Langerhans and histiocytic cells 2,3. The function, ultrastructure, morphology and immunostaining of these cells are different. Whereas follicular, interdigitating and Langerhans cells have an important function in the immune system and play a key role in antigen presentation to lymphocytes, histiocytic (fibroblastic) cells are thought to be responsible for the stromal structure of lymph nodes. These cells can be distinguished by a combination of morphological and immunophenotypic features. According to the World Health Organization (WHO) classification, DCNs are included among the histiocytic and dendritic cell neoplasms 4. DCNs are classified by the International Lymphoma Study Group into 4 major immunophenotypic groups: histiocytic sarcoma, Langerhans cell tumor/sarcoma (LCT/LCS), interdigitating dendritic cell tumor/sarcoma (IDDCT/IDD- CS), and follicular dendritic cell tumor/sarcoma FDCT/FDCS (Table 1) 3. DCNs can occur in lymph nodes and extranodal sites, the latter accounting for one-third of DCNs 3,5. However, data on DCNs are mostly based on single case reports or case series and their natural history and standard treatment are not clear yet. To increase the understanding of this rare disease, we report our experience of 3 cases of FDCS with an analysis of the morphological and immunophenotypic characteristics, clinical course, treatment options and response to treatment. In addition, we have reviewed the literature on DCNs. Case 1 A 43-year-old female patient was admitted to hospital with complaints of abdominal pain. She did not have constitutional symptoms. There was no significant personal or family history. The patient s physical and routine laboratory examination results were normal. Abdominal ultrasonography (US) revealed a well-defined, Key words: dendritic cell neoplasms, follicular dendritic cell sarcoma. Correspondence to: Yuksel Urun, MD, Department of Medical Oncology, Ankara University School of Medicine, Cebeci Hospital 06590, Dikimevi/ Ankara, Turkey. Tel ; fax ; yukselurun@gmail.com Received February 28, 2012; accepted June 4, 2012.
2 e66 Table 1 - Classification of histiocytic and denditric cell neoplasms Macrophage/histiocytic neoplasm Histiocytic sarcoma Dendritic cell neoplasm Langerhans cell histiocytosis Langerhans cell sarcoma Interdigitating dendritic cell sarcoma/tumor Follicular dendritic cell sarcoma/tumor Dendritic cell sarcoma, not otherwise specified Modified from Kairouz et al., ; Pileri et al., ; Swerdlow et al., ; De Pas et al., mm, hypoechoic solid mass with foci of calcification in the right adrenal region. Computed tomography (CT) scan was similar to the US findings. A heterogeneously enhancing mass lesion with regular margins and containing calcifications was observed adjacent to the head of the pancreas at the level of the descending part of the duodenum. In January 2009 a right adrenalectomy was performed and the mass was totally removed. Intraoperatively the tumor was cm, mobile, and adjacent to the pancreas and duodenum. It extended into the surrounding tissue and there was an adjacent enlarged (10 10 mm) lymph node. Histopathological and immunohistochemical evaluation showed a tumor size of cm. Abundant small lymphocytes were noticed between tumor cells and around the vascular structures. Some of the cells showed expression of Epstein-Barr virus (EBV). Diffuse CD21 and CD35 and focal CD23 positivity was observed. Also fascin, CD68, CD20 and LCA were positive. S-100, CD30, CD34 and actin were negative. The ki-67 proliferation index was 5-15% (Table 2). A diagnosis of FDCS was made. PET/CT scan was done for staging in March It revealed increased FDG uptake in the paravertebral area at the level of L3 in some lymph nodes (the largest 10 mm with SUV max 3.44). Adjuvant chemotherapy was planned by our oncology team and 6 cycles of CEOP (cyclophosphamide, epirubicin, vincristine and prednisolone) were administered. Posttreatment PET/CT showed no abnormalities. The patient was last evaluated in April Thoracoabdominopelvic CT was normal and the patient was in complete remission after 32 months of completing treatment. Case 2 Y URUN, D KANKAYA, L KORAL ET AL A 45-year-old male patient was admitted in September 1997 because of rectal bleeding. Systemic examination including digital rectal examination and routine laboratory values were within normal limits. The patient s personal and family history was unremarkable. Rectoscopic evaluation was done and endoscopic examination revealed a polypoid mass at 10 cm. Histopathological examination of the endoscopic biopsy reported a malignant melanoma. During laparotomy a tumor invading the surrounding tissues was seen that was considered inoperable, so a colostomy was created. The response to 2 cycles of cisplatin and dacarbazine was stable disease. The subsequently administered combination of vincristine, bleomycin, CCNU and interferon produced no response. Pelvic radiotherapy in 10 fractions for a total dose of 30 Gy was administered in July 1998 after the failure of chemotherapy. The patient was then lost to follow-up. The patient presented again with complaints of rectal pain and discharge in April Physical examination and laboratory findings were within normal limits. A submucosal ulcerated lesion of 2 cm in diameter was detected at rectoscopy. Endorectal US showed increased rectal wall thickness reaching 8 mm in some areas. PET/CT scan showed distal intestinal system involvement with SUV max values of Endoscopic rectal biopsy was performed again and histopathological examination revealed a tumor consisting of spindle to ovoid cells arranged in short fascicles. Immunohistochemical staining was performed with a wide panel of antibodies. Tumor cells only showed vimentin positivity while pancytokeratin, S- 100, desmin, smooth muscle actin, myogenin, CD117, CD34, HMB-45 and Melan A were negative. The mass was diagnosed as a malignant mesenchymal tumor. Low anterior resection was performed in November Macroscopic examination of the specimen revealed a circumscribed nodule which was 4 cm in longest diameter and located in the submucosa and muscularis propria of the nonperitonealized region of the rectum. Its cut surface was solid and had a white color with foci of hemorrhage. Microscopically, spindle to ovoid cell proliferation forming fascicles, whorls and Table 2 - Immunohistochemical features of 3 patients with follicular dendritic cell sarcoma (FDC) Cases CK SMA vim EMA CD45 CD21 CD23 CD34 CD35 pod fascin CD68 CD117 S-100 HMB-45 Ki-67 EBER (%) 1 NT NT NT NT NT NT + + NT - NT NT NT NT NT NT NT vim, vimentin; pod, podoplanin; EBER, EBV-encoded RNA; NT, not tested.
3 INTRAABDOMINAL FOLLICULAR DENDRITIC CELL SARCOMA e67 A B C D E F Figure 1 - Pathological evaluation of case 2. A) Well circumscribed nodule located in the submucosa and muscularis propria of the rectum ( 4). B) Spindle or ovoid cells with indistinct cell borders form fascicles, whorls and a storiform pattern ( 10). C, D) Diffuse vimentin and CD21 positivity in the tumor cells ( 10, 20). E) CD20- positive B lymphocytes surrounding tumor cells ( 10). F) Ki-67 proliferation index was about 5-10% ( 20). a storiform pattern was seen (Figure 1A, 1B). The tumor cells had vesicular nuclei with finely dispersed chromatin and distinct small nucleoli. They had plump, eosinophilic cytoplasm with indistinct cell borders. The mitotic count was 3 per 10 HPFs. The surgical margins and regional lymph nodes were free of tumor. Immunohistochemically the tumor cells showed strong, diffuse CD21 and CD23 expression and vimentin expression (Figure 1C, 1D). There was a population of CD20-positive B lymphocytes accompanying the neoplastic cells (Figure 1E). The Ki-67 proliferation index was about 5-10% (Figure 1F). The tumor was diagnosed as an FDCS. In situ hybridization for EBV was negative. The colostomy was repaired by general surgery. No adjuvant chemo- or radiotherapy was administered. The patient is still in complete remission at 21 months follow-up. Case 3 A 24-year-old male patient was admitted to the hospital in January 2009 with a 3-month history of abdominal pain, fever, night sweats and weight loss. Physical examination and routine laboratory values were within normal limits except a slight increase in LDH and ESR. The patient s personal and family history was unremarkable. US showed multiple hypoechoic lesions in the liver, the largest measuring 12 mm, and multiple enlarged abdominal lymph nodes. Abdominal CT scan showed no detectable mass in the liver but a solid mass of mm at the level of the right psoas muscle. The patient was free of complaints for 4 months but was readmitted to our clinic with complaints of abdominal pain, fever, night sweats and weight loss in June Tomographic examination revealed multiple hypo-
4 e68 dense lesions with peripheral contrast enhancement in the liver and paraaortic paracaval lymph nodes, the largest measuring mm and 40 mm, respectively. Upper gastrointestinal endoscopic examination was normal except for erythematous gastritis. Liver biopsy was performed and pathological examination showed that tumor had replaced large portions of the liver parenchyma. The tumor cells had spindle-shaped nuclei and showed rare mitoses. The cell borders were ill-defined and showed a syncytial growth pattern and there were eosinophils between tumor cells. Initially a diagnosis of malignant mesenchymal tumor or lymphoma was considered but immunohistochemistry revealed that the tumor was positive for CD117 and negative for S-100, desmin and actin, so a diagnosis of gastrointestinal stromal tumor (GIST) was made. Multiple liver lesions and metastatic abdominal lymph nodes were found on PET/CT with an SUV max of Treatment with imatinib 400 mg/day was initiated. When after 2 months no response was observed another liver biopsy was done. Histopathologically, a differential diagnosis between germ cell tumor, lymphoma and malignant mesenchymal tumor was considered. Because the patient s performance status had deteriorated, combination therapy with cisplatin 20 mg/m 2 and etoposide 100 mg/m 2 for 3 days was administered, resulting in a subjective response. Immunohistochemical staining showed positivity for vimentin, fascin, CD68, CD21 and CD23, and negativity for MPO, CD45, panck, CK8/18, EMA, PLAP, CD117, HMB-45, S-100, SMA, CD30, ALK-1, CD1a, BHCG, podoplanin, CD4, CD8, CD10, and bcl-2, while Ki-67 was 40-50% (Table 2). A diagnosis of FDCS was made. CT scan after the second cycle of cisplatin and etoposide revealed an 80% reduction of the lesions. An additional 2 cycles of cisplatin-etoposide were given but there was rapid progression of disease. Third-line chemotherapy was planned but the patient died shortly after, 5 months after the diagnosis of FDCS. Discussion DCNs are rare tumors that are being diagnosed with increasing frequency. They affect both sexes more or less equally. The median age in the literature was years (range, 2 days to 83 years). Although most of these tumors localize in lymph nodes, especially in the cervical, mediastinal and axillary regions, approximately one-third of cases involve extranodal sites. Constitutional symptoms are not common 3,6-8. There is no definitive etiology for most FDCSs. It is known that FDCS expresses the EBV receptor CD21 and EBV has been documented in some cases. In these cases EBER in situ hybridization was positive. However, the role of EBV remains unclear. Castleman disease has been found in association with FDCS 2,5,7,9. In our series, case 2 had a history of radiotherapy administered 11 Y URUN, D KANKAYA, L KORAL ET AL years before the diagnosis of FDCS. Nevertheless, there are no data available about the role of radiotherapy. The clinical presentation varies depending to the location of the primary tumor. The size of FDCS in the literature was variable (1-21 cm) 5,7. Most studies of FDCS focused on morphological, immunohistochemical and etiological features and little emphasis has been placed on the imaging findings of this tumor. Kang et al. 10 reported the imaging findings of 2 cases of abdominal FD- CS. Both cases manifested as a discrete, well enhancing homogeneous mass with internal necrosis and regional lymphadenopathy. Internal calcification was another feature and the sizes were 5 and 12 cm. Long-Hua et al. 11 reported imaging findings of 4 cases of FDCS between 1.5 and 15 cm in size. The tumor margins of their cases were generally well defined and CT attenuation was variable: the tumors demonstrated relatively homogeneous attenuation but an abdominal lesion showed heterogeneous attenuation. The tumors of our first and third cases measured mm and mm, respectively. CT evaluation of the first case showed a heterogeneously enhancing mass lesion with regular margins and containing calcifications. Tomographic examination of the third patient revealed multiple hypodense lesions with peripheral contrast enhancement in the liver and paraaortic paracaval lymph nodes, but there was no calcification. We also performed PET/CT in our cases and the SUV max values were between 3 and 14. Therefore, our opinion is that FDCS can have variable radiological features that are generally nonspecific. FDCS is often histologically confused with inflammatory pseudotumor, mesenchymal tumor (especially GIST in the case of intraabdominal tumors), lymphoid neoplasms, melanoma, and carcinoma 2,9,12. Most patients were positive for CD21, CD23, CD35 and CD68 3,7 and negative for CD1a. The mean Ki-67 was around 10-20% (range, 1-60%) 3,7,13. Because FDCS are rare tumors, assessment of their prognosis is difficult. Nevertheless, tumor size >5 cm, intraabdominal location, high mitotic index ( 5/10 HPF), high histological grade and coagulative necrosis have been proposed as predictors of an unfavorable clinical course 5,8. Consistent with this, patient 3 in our series with an abdominal tumor experienced a dismal clinical course and died shortly after the diagnosis. However, the currently available information is still insufficient to allow any assessment of the clinical significance of morphological or biological features. Likewise, the prognostic role of Ki-67 is not fully understood but in our series Ki-67 was 5-15% in both patients with localized disease and 40-50% in the patient with metastatic and progressive disease. Surgery, radiotherapy, chemotherapy or combinations of these treatments have been used with different outcomes. In patients with localized disease, the mainstay of treatment is surgery. In the reported series in the literature, surgery without any adjuvant treatment was
5 INTRAABDOMINAL FOLLICULAR DENDRITIC CELL SARCOMA curative in approximately half of patients. However, the rate of relapse approaches 40% in patients who were treated with surgery alone 7,8. Adjuvant radiotherapy was observed to prolong the disease-free survival in some reports. Nonetheless there have been divergent results of adjuvant or neoadjuvant chemotherapy and radiotherapy 8. Most regimens that have been used for FDCS were typical lymphoma regimens (CHOP: cyclophosphamide, doxorubicin, vincristine, prednisone; ABVD: doxorubicin, bleomycin, vinblastine, dacarbazine). Even in FDCSs with an indolent course, fatal outcomes have been reported 2,14. Patients presenting with metastatic disease or relapse had a poor prognosis. Several chemotherapy combinations have been used with limited success 2. Azim et al. 15 obtained a complete response with chemotherapy (cisplatin and gemcitabine) plus imatinib in a patient with positivity for CD117 and abdominal and mediastinal involvement. However, in our case 3, which was CD117 positive, imatinib did not have any beneficial effect. Thus, single-agent imatinib may have limited effect but in combination with appropriate chemotherapy it may be useful. In summary, DCNs are rare tumors that should be considered in the differential diagnosis of sarcomas and lymphomas. Although the number of reported cases has increased in recent years, for an optimal evaluation and treatment approach more data are needed. References e69 1. Monda L, Warnke R, Rosai J: A primary lymph node malignancy with features suggestive of dendritic reticulum cell differentiation. A report of 4 cases. Am J Pathol, 122: , Kairouz S, Hashash J, Kabbara W, McHayleh W, Tabbara IA: Dendritic cell neoplasms: an overview. Am J Hematol, 82: , Pileri SA, Grogan TM, Harris NL, Banks P, Campo E, Chan JK, Favera RD, Delsol G, De Wolf-Peeters C, Falini B, Gascoyne RD, Gaulard P, Gatter KC, Isaacson PG, Jaffe ES, Kluin P, Knowles DM, Mason DY, Mori S, Müller-Hermelink HK, Piris MA, Ralfkiaer E, Stein H, Su IJ, Warnke RA, Weiss LM: Tumours of histiocytes and accessory dendritic cells: an immunohistochemical approach to classification from the International Lymphoma Study Group based on 61 cases. Histopathology, 41: 1-29, Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (Eds): WHO classification of tumours of haematopoietic and lymphoid tissues. World Health Organization, IARC Press, Lyon, Li L, Shi YH, Guo ZJ, Qiu T, Guo L, Yang HY, Zhang X, Zhao XM, Su Q: Clinicopathological features and prognosis assessment of extranodal follicular dendritic cell sarcoma. World J Gastroenterol, 16: , Wang H, Su Z, Hu Z, Wen J, Liu B: Follicular dendritic cell sarcoma: a report of six cases and a review of the Chinese literature. Diagn Pathol, 5: 67, Soriano AO, Thompson MA, Admirand JH, Fayad LE, Rodriguez AM, Romaguera JE, Hagemeister FB, Pro B: Follicular dendritic cell sarcoma: a report of 14 cases and a review of the literature. Am J Hematol, 82: , De Pas T, Spitaleri G, Pruneri G, Curigliano G, Noberasco C, Luini A, Andreoni B, Testori A, de Braud F: Dendritic cell sarcoma: an analytic overview of the literature and presentation of original five cases. Crit Rev Oncol Hematol, 65: 1-7, Youens KE, Waugh MS: Extranodal follicular dendritic cell sarcoma. Arch Pathol Lab Med, 132: , Kang TW, Lee SJ, Song HJ: Follicular dendritic cell sarcoma of the abdomen: the imaging findings. Korean J Radiol, 11: , Long-Hua Q, Qin X, Ya-Jia G, Jian W, Xiao-Yuan F: Imaging findings of follicular dendritic cell sarcoma: report of four cases. Korean J Radiol, 12: 122, Romero-Guadarrama MB, Reyes-Posada O, Hernandez-Gonzalez MM, Duran-Padilla MA: Follicular dendritic cell sarcoma/tumor: 2 cases of a rare tumor of difficult clinical and pathological diagnosis. Ann Diagn Pathol, 13: , Orii T, Takeda H, Kawata S, Maeda K, Yamakawa M: Differential immunophenotypic analysis of dendritic cell tumours. J Clin Pathol, 63: , Cyriac S, Praveenkumar D, Majhi U, Sagar TG: Follicular dendritic cell sarcoma of the neck with an aggressive and fatal course. J Cancer Res Ther, 6: , Azim HA, Elsedewy E, Azim HA, Jr: Imatinib in the treatment of follicular dendritic sarcoma: a case report and review of literature. Onkologie, 30: , 2007.
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