Magn Reson Med Sci, Vol. 14, No. 4, pp. 347–354, 2015
doi:10.2463/mrms.2014-0052
© 2015 Japanese Society for Magnetic Resonance in Medicine
CASE REPORT
Inflammatory Pseudotumor-like Follicular Dendritic Cell Tumor of the Spleen: Case Report and Review of the Literature Yoshiyuki KITAMURA1, Yukihisa TAKAYAMA2, Akihiro NISHIE1*, Yoshiki ASAYAMA1, Yasuhiro USHIJIMA1, Nobuhiro FUJITA1, Koichirou MORITA1, Shingo BABA1, Yuichiro KUBO3, Ken SHIRABE4, and Hiroshi HONDA1 1
Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University 3–1–1 Maidashi, Higashi-ku, Fukuoka 812–8582, Japan 2 Department of Radiology Informatics and Network, Graduate School of Medical Sciences, Kyushu University 3 Department of Anatomic Pathology, Graduate School of Medical Sciences, Kyushu University 4 Department of Surgery and Science, Graduate School of Medical Sciences, Kyushu University (Received May 1, 2014; Accepted October 29, 2014; published online February 12, 2015)
A 74-year-old woman underwent contrast-enhanced (CE) computed tomography (CT) that revealed an enlarging splenic lesion. This splenic tumor was suspected as metastasis because the patient had been diagnosed with right breast cancer with lung and right axillary lymph node metastases 4 years earlier and had undergone surgery and hormone therapy at another hospital. T 2 -weighted imaging of magnetic resonance (MR) imaging demonstrated the tumor with slightly high intensity with a rim of low intensity at the margin. On dynamic contrast-enhanced (DCE)-MR imaging after intravenous administration of gadolinium diethylenetriamine pentaacetic acid, delayed enhancement was observed in the center and margin of the tumor. On positron emission tomography with 2-deoxy-2-[18F] fluoro-Dglucose (FDG) integrated with CT, the tumor showed high FDG uptake. Splenic metastasis was considered based on the imaging findings, lack of inflammation on laboratory data, and clinical course, so she underwent splenectomy. Histopathologically, the tumor was encapsulated by a fibrous structure, which was depicted as the rim at the tumor margin on T 2 -weighted imaging and DCE-MR imaging. Immunohistochemical study allowed the diagnosis of inflammatory pseudotumor (IPT)-like follicular dendritic cell tumor (FDCT). FDCT is a primary neoplasm of lymph nodes that shows features of follicular dendritic cell differentiation, and it is rare at the spleen. Differential diagnosis is difficult between IPTlike FDCT and similar splenic tumors, such as IPT, splenic metastases, hamartoma and hemangioma. However, in addition to the enhancement pattern within a tumor on DCEMR imaging, detection of the capsular-like rim on MR imaging might aid the diagnosis of splenic IPT-like FDCT. Keywords: Epstein-Barr virus, follicular-dendritic cell tumor (FDCT), MRI, spleen stein-Barr virus (EBV) infection and are referred to as inflammatory pseudotumor (IPT)-like FDCTs because they resemble IPTs histologically. 3–5 Several reports provide imaging findings of splenic FDCTs on computed tomography (CT) and/or magnetic resonance (MR) imaging 6 –12 and describe the lesions as well circumscribed with delayed enhancement. 7,10 These imaging features resemble those of other splenic tumors, such as metastatic tumors, lymphomas, and IPTs, so preoperative diagnosis of FDCTs is difficult. 8 One pathological feature of
Introduction Follicular dendritic cell tumors (FDCTs) are primary neoplasms of the lymph nodes that show features of follicular dendritic cell differentiation. 1 More than 70% of FDCTs occur at the lymph node(s), and 8% of FDCTs occur in the spleen. 2 Splenic FDCTs are generally associated with Ep*Corresponding author, Phone: +81-92-642-5695, Fax: +8192-642-5708, E-mail: [email protected] 347
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FDCTs is the presence of a fibrous capsule between the tumor and the surrounding parenchyma. 4,6 To the best of our knowledge, the presence of capsular formation has rarely been referenced in the differential diagnoses of splenic tumors. The radiological detection of this capsule might be helpful to differentiate splenic IPT-like FDCTs from other splenic tumors. We report a case of a splenic IPT-like FDCT that showed MR findings suggestive of a fibrous capsule, and we discuss the utility of this finding in diagnosing splenic tumors.
Case Report A 74-year-old woman was admitted to our hospital 4 years after she was diagnosed with right breast cancer with lung and right axillary lymph node metastases and underwent surgery and hormone therapy at another hospital. During the course of follow-up after her right mastectomy, contrastenhanced (CE) CT demonstrated a splenic tumor. CE-CT was performed with a 64-row multidetector CT unit (Aquilion 64, Toshiba Medical Systems, Tokyo, Japan) using parameters: 120 kVp, 100 to 300 mAs, 0.5-mm collimation, 0.828 pitch factor, and a single breath-hold helical acquisition of 5 to 8 s, depending on liver size. Using these raw data, transverse images were obtained with a slice thickness of 5 mm and no slice gap. The patient received intravenous administration of a total of 2.0 mL/kg (maximum, 100 mL) of nonionic iodinated contrast agent (Iopamilon 370, 370 mgI/mL, Bayer HealthCare, Osaka, Japan) at a rate of 3.0 mL/s using an automatic injector (Nemoto Kyorindo, Tokyo, Japan). Images scanned 43 s (early phase), 70 s (portal phase) and 240 s (delayed phase) after the beginning of contrast agent administration were used for assessment. The tumor diameter was 15 mm at that time and increased to 29 mm within 10 months. The patient visited our hospital for further evaluation. She had no symptoms. Laboratory tests including complete blood count, blood serum chemistry, and tumor markers (e.g., cancer antigens 15– 3, 19–9, and 125 and C-reactive protein) were within normal limits. The well circumscribed splenic tumor showed similar density to that of the spleen (Fig. 1a) without calcification and inhomogeneous and weak enhancement on early phase image (Fig. 1b). The splenic tumor showed delayed enhancement according to portal- and delayed-phase images (Fig. 1c, d), and the delayed-phase image showed an area of low density within the tumor. She underwent MR imaging for detailed evaluation of the splenic tumor using a 3-tesla MR system. Table 1 details the MR sequence parameters. On in-
Fig. 1. Images of (a) precontrast-enhanced, (b) early, (c) portal, and (d) delayed phases. The early phase was scanned 43 s, portal phase, 70 s, and delayed phase, 240 s after the beginning of contrast agent administration. The well circumscribed splenic tumor showed similar density to the spleen on precontrastenhanced computed tomography (CT) (a) and inhomogeneous and slight enhancement on early-phase image (b). The tumor showed delayed enhancement according to portal- and delayed-phase images (c, d). There was an area of low density within the tumor on delayed-phase image. In this contrast-enhanced (CE) CT image, the tumor diameter was 29 mm.
phase T 1 - (T 1 WI) and fat-suppressed T 2 -weighted imaging (FS-T 2 WI), the signal intensity of the tumor resembled that of the spleen parenchyma (Fig. 2a, b), and a rim of low intensity was depicted at the margin of the tumor (Fig. 2b). On diffusionweighted imaging (DWI) of b-value 1,000 mm2 /s, signal intensity of the tumor was slightly high, but that of the margin of the tumor was low compared with that of the spleen parenchyma (Fig. 2c). The apparent diffusion coefficient (ADC) of the tumor, 0.98 © 10 ¹3 mm 2 /s, was slightly higher than that of the spleen parenchyma, 0.86 © 10¹3 mm2/s (Fig. 2d). On dynamic contrast-enhanced (DCE) MR imaging, signal intensity of the tumor was similar to that of the spleen parenchyma on pre-contrast images (Fig. 3a). After intravenous administration of gadolinium diethylenetriamine pentaacetic acid (GdDTPA, Magnevist, Bayer Healthcare, Osaka, Japan), the tumor showed inhomogeneous and weak enhancement 25 s after contrast introduction (Fig. 3b) and similar enhancement 90 s after contrast introMagnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
Table 1.
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Details of the magnetic resonance (MR) sequence parameters
Parameters
Unit
T1WI (CSI)
ssT2WI
DWI
DCE-MRI
Repetition time Echo time Flip angle Field of view Matrix (frequency © phase) Slice thickness Slice gap Number of slices Number of excitations Fat suppression Respiratory control Band width Scan time of whole slices
(ms) (ms) (degrees) (mm)
160.0 1.15/2.27 60 380 © 329 240 © 207 7.0 1.0 25 1 No Breath-hold 1898.5 00:14.8
1154.0 71.0 90 380 © 299 112 © 88 7.0 1.0 25 1 SPAIR Breath-hold 569.6 00:30.0
1867.0 55.0 90 380 © 299 112 © 88 7.0 1.0 25 1 SPIR Triggered 99.5 01:39.0
3.0 1.4 10 375 © 298 252 © 200 3.0 ¹1.5 133 1 SPAIR Breath-hold
(mm) (mm)
(Hz/pixel) (min:sec)
723.4 17.9
T1WI: T1-weighted imaging, CSI: chemical shift imaging, ssT2WI: single-shot T2-weighted imaging, DWI: diffusionweighted imaging, DCE-MRI: dynamic contrast-enhanced magnetic resonance imaging, SPIR: spectral presaturation with inversion recovery, SPAIR: spectral attenuated with inversion recover
duction (Fig. 3c) compared with the spleen parenchyma. On delayed-phase image obtained 240 s after the administration of Gd-DTPA, the center and margin of the tumor showed enhancement even though other parts of the tumor and the spleen parenchyma showed washout (Fig. 3d). The unenhanced area within the tumor was suspected to represent degenerative change or necrosis. On positron emission tomography with 2-deoxy-2-[18F] fluoro-D-glucose integrated with CT ( 18 F-FDG-PET/CT), the tumor showed high FDG uptake with a maximum standardized uptake value (SUVmax) of 14.3 (Fig. 4). There was no abnormal uptake in any other organ, including the liver, breasts, lungs, and lymph nodes. A malignant tumor including splenic metastasis was considered based on the clinical course, high FDG uptake, and lack of inflammation, so a splenectomy was performed to confirm the diagnosis and clarify a treatment strategy. The tumor measured 36 © 35 mm on gross specimen and histologically comprised a proliferation of lymphocytes, histiocytes, plasma cells, and fibroblastic cells. We also observed many epithelioid cell granulomatous lesions and scattered oval- to spindle-shaped cells with irregular nuclei and identified a fibrous structure between the tumor and the splenic parenchyma (Fig. 5a). Immunohistochemically, the infiltrating oval- to spindle-shaped cells were positive for fascin but negative for CD21, CD35, anaplastic lymphoma kinase (ALK), Epstein-Barr virus latent membrane protein (EBV-LMP), and Epstein- Barr virus nuclear antigen antibody (EBNA). EpsteinBarr virus-encoded small RNA (EBV-EBER) was Vol. 14 No. 4, 2015
positive by in situ hybridization (Fig. 5b). Although FDC markers were negative, these histological features suggested IPT-like FDCT. Two years after the splenectomy, the patient was alive and showed no evidence of recurrent disease.
Discussion FDCT is a rare neoplasm classified as a histiocytic and dendritic neoplasm. 13 Monda and associates reported this tumor first in 1986 as a primary neoplasm of lymph nodes that showed features of follicular dendritic cell (FDC) differentiation. 1 A malignant proliferation of FDCT is called a follicular dendritic cell sarcoma. 14 FDCs normally act as antigen-presenting cells for B cells and promote Bcell proliferation and differentiation. 14 FDCTs are thought to occur mainly at lymph nodes, most commonly in the cervical and axillary regions. 15 The tumor may also occur at various extranodal sites, such as the palate, pharynx, tonsil, thyroid, mediastinum, gastrointestinal tract, liver, and spleen as a slow-growing, well circumscribed, and painless mass. 2 The symptoms of FDCTs, such as low grade fever, weight loss, epigastralgia, abdominal fullness, and slight anemia, are nonspecific. The diagnosis of FDCT is usually made by histological examination. Histologically, FDCTs are characterized by the syncytial growth of spindle or ovoid cells, which are immunoreactive for such various FDC markers as CD21 and CD35. 4 A storiform or whorled growth pattern is frequently encountered. 3
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Fig. 2. (a) In-phase T1-weighted imaging (T1WI), (b) fat-suppressed T2-weighted imaging (FS-T2WI), (c) diffusion-weighted imaging (DWI) of b-value with 1,000 mm2/s, and (d) apparent diffusion coefficient (ADC) map of magnetic resonance (MR) imaging. The signal intensity of the splenic tumor was similar to that of the spleen parenchyma on T1WI and FST2WI (a, b). The tumor showed slightly higher signal intensity than the spleen parenchyma on DWI. The tumor demonstrated a rim of low intensity on FST2WI and DWI (b, c). The ADC value of the tumor, 0.98 © 10¹3 mm2/s, was slightly higher than that of the spleen parenchyma, 0.86 © 10¹3 mm2/s (d).
Fig. 3. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) (a) pre-enhancement and (b) 25, (c) 90, and (d) 240 s after the administration of gadolinium diethylenetriamine pentaacetic acid (GdDTPA). Signal intensity of the splenic tumor was similar to that of the spleen parenchyma on pre-contrast images (a). The tumor showed inhomogeneous and weak enhancement (b) and similar enhancement (c) compared with that of the spleen parenchyma. The tumor showed delayed enhancement at the center and margin of the tumor (d). Delayed enhancement at the margin of the tumor was considered the rim (d). The unenhanced area within the tumor was suspected to represent degenerative change or necrosis (d).
FDCTs are categorized into 2 types–conventional FDCTs composed of the storiform, fascicular, and diffuse growth of tumor cells with a sprinkling of lymphocytes and IPT-like FDCTs composed of dispersed tumor cells with intense lymphocytes and plasma cells. 4 EBV-positive IPT is sometimes used instead of IPT-like FDCT to refer to this entity, but EBV-positive IPT and IPT-like FDCT may be considered the same disease entity, although more discussion is required. 8 Most FDCTs arising at the liver or spleen are categorized as IPT-like FDCTs, and this type is rare at other sites. 4 IPT-like FDCTs arising at the liver or spleen are associated with EBV infection, whereas conventional FDC tumors show EBV association in only one of 25 cases (4%). 3–5 Thus, the identification of EBV infection is important in the diagnosis of IPT-like FDCTs by immunostaining for EBV-LMP, which is a protein product
of EBV with transforming function, or by the detection of the EBER gene by in situ hybridization. 4 Other clinicopathologic features of IPT-like FDCT that differ from those of conventional FDCT include female predilection, occurrence in intra-abdominal sites, systemic inflammatory symptoms such as weight loss and fever, indolent clinical course such as less frequent recurrence, and metastasis. 4 Complete surgical resection is the first choice to treat IPT-like FDCTs because they are thought to have a low-to-intermediate malignancy potential despite an indolent clinical course. 4 Systemic chemotherapy and radiotherapy have also been used as treatment methods, but their efficacy in improving patients’ survival rate is not established. A long follow-up is also necessary for IPT-like FDCTs after treatment. 4 Only 19 cases of splenic IPT-like FDCTs or IPTs Magnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
with EBV positivity have been reported. 2,4,6 –12 Ten of 19 cases have been described their imaging findings (Table 2). 6–12 Of them, CT findings were described in 8 cases, all of which showed a well circumscribed margin. CE-CT in 7 cases showed heterogeneous enhancement. 7,8,10 –12 MR imaging was performed in 2 cases. 8,10 Tumors in the previous reports showed isointensity on T 1 WI, low intensity on T 2 WI, and homogenous or heterogeneous delayed enhancement on DCE-MR imaging. The T 1 WI and DCE-MR imaging findings for our patient were consistent with those reported previously. 8,10 Delayed enhancement of an IPT-like FDCT on CE-CT and DCE-MR imaging is a satisfactory finding because of its similar histology with that of IPT. However, our patient’s tumor showed slightly high signal intensity on T 2 WI, which was inconsistent with the signal intensity of the previous cases. IPTs show variable signal intensity on T 2 WI according to their constituent contents. 5 This difference in T 2 signal intensity may be due to the amount of inflammatory and/or spindle fibrosis within each tumor. Our patient’s T 2 WI depicted a rim of low intensity at the margin of the tumor. This rim was also shown with delayed enhancement on DCE-MR imaging. In the comparison with the histological
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Fig. 4. Fusion image of positron emission tomography with 2-deoxy-2-[18F] fluoro-D-glucose integrated with computed tomography ( 18F-FDG-PET/CT). The splenic tumor showed high FDG uptake with a maximum standardized uptake value (SUVmax) of 14.3.
Fig. 5. (a) Macroscopic and (b) microscopic graphs of the specimen from the spleen. Microscopic graph (hematoxylin and eosin stain ©40) showed that the tumor (T) comprised a proliferation of lymphocytes, histiocytes, plasma cells, and fibroblastic cells accompanied by many epithelioid cell granulomatous lesions and scattered oval- to spindleshaped cells with irregular nuclei. A fibrous structure (arrows) was identified between the tumor (T) and the splenic parenchyma. (c) FS-T2WI of the spleen (same image as Fig. 2b). (d) Epstein-Barr virus-encoded small RNA (EBVEBER) was positive by in situ hybridization (©400). Vol. 14 No. 4, 2015
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Table 2.
Summary of the reported cases of splenic follicular dendritic cell tumor (FDCT) including imaging findings Tumor size (cm)
Case No.
Age (yrs)/ Sex
1
54/M
2
64/M
n/a
3
56/F
4
4
60/M
2
5
78/F
3
6 7
44/F 39/M
11 © 8 8
8
78/F
7 © 7.5
9
77/F
10
74/F
Findings of computed tomography (CT)*
12 © 17 Low attenuation on CT (images not available) Heterogeneous weak enhancement on contrastenhanced (CE) CT Heterogeneous weak enhancement on CE-CT
Heterogeneous weak enhancement on CE-CT Heterogeneous weak enhancement on CE-CT Cystic tumor Heterogeneous delayed enhancement on CE-CT
Heterogeneous enhancement on CE-CT 11 © 9©9 Heterogeneous enhancement with area of low density at the center of the tumor on CE-CT 3.6 © 3.5 Heterogeneous delayed enhancement with area of low density within the tumor on CE-CT
Findings of magnetic resonance imaging (MRI)*
Histopathological findings of the capsular-like rim
n/a
Surrounded by fibrous tissue with a low number of fibroblasts n/a
n/a
Our review of the imaging Ref. findings of the capsular-like rim n/a
(6)
Nonidentifiable
(7)
Iso-signal intensity on T1WI, low signal intensity on T2WI, and delayed enhancement on DCE-MRI n/a
n/a
Identifiable on T2WI
(8)
n/a
Nonidentifiable
(8)
n/a
n/a
Nonidentifiable
(8)
n/a n/a Marked low signal n/a intensity on T1WI and T2WI and delayed enhancement on DCE-MRI n/a n/a
Nonidentifiable Nonidentifiable
(9) (10)
Nonidentifiable
(11)
n/a
n/a
Nonidentifiable
(12)
Iso-signal intensity on T1WI and T2WI and delayed enhancement on DCE-MRI
Fibrous structure at part of the tumor circumference
Identifiable on T2WI and DCE-MRI
Our case
*Attenuations at CE-CT and signal intensities at MRI of the splenic FDCTs are compared with those of the spleen parenchyma. n/a, not available; DCE-MRI, dynamic contrast-enhanced MRI; Ref., reference number; T1WI, T1-weighted imaging; T2WI, T2-weighted imaging
findings, a fibrous structure demarcated the tumor from the spleen parenchyma. This fibrous structure would probably be demonstrated as an imaging finding. The previous reports seem to describe the capsular-like rim at the margin of IPT-like FDCTs, although the authors do not mention it specifically. 8,10 In our case, difficult depiction of the capsu-
lar-like rim on CE-CT was possibly related to low contrast between lesion and nonlesion between the capsular-like rim and spleen parenchyma. Thus, MR imaging is more advantageous than CT for evaluating the capsular-like rim at the margin of IPT-like FDCT. Histologically, it is known that IPT-like FDCTs Magnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
occasionally show a peritumoral fibrous capsule. These tumors are well circumscribed and show expansive growth. 6 The frequency of a capsular-like rim of the splenic IPT-like FDCT is unknown. We could evaluate the capsular-like rim of a splenic IPT-like FDCT in only one previous report, but the authors did not discuss it. 6 Our report is the first to mention imaging findings of this capsular-like rim. The peritumoral fibrous capsule might be the secondary product of an interaction between the tumor and the host spleen, which might be the similar interaction between a hepatocellular carcinoma and the host liver. 16 A tumor showing delayed enhancement and a capsular-like rim simultaneously would be extremely rare. Splenic metastases show usually minimal to heterogeneous centripetal enhancement that depends on the primary neoplasm. 17 Pathological findings of splenic metastases have also been reported. 18 However, we found no report concerning the peritumoral fibrous capsule of splenic metastases. The radiological detection of this capsule might be helpful to differentiate splenic IPT-like FDCTs from other splenic tumors, although more discussion is required to clarify the clinical utility of the finding. Other important differential diagnoses of splenic tumors that show delayed enhancement are hamartoma and hemangioma. These tumors do not show the capsular-like rim because their growth is very slow, so the peritumoral fibrous capsule rarely occurs. 19 Therefore, the combination of delayed enhancement and a capsular-like rim may be imaging findings that help us differentiate IPT-like FDCTs from other splenic tumors. Only one case report described 18 F-FDG-PET/ CT findings of a follicular dendritic cell sarcoma, but not FDCT. In that report, the tumor showed high FDG uptake. 11 Our patient’s IPT-like FDCT also showed high FDG uptake, but 18 F-FDG-PET or PET/CT may not be helpful for the differentiation of IPT-like FDCT from other splenic tumors because some splenic tumors, such as metastatic tumors or lymphomas, can also show high FDG uptake. 20 Further evaluation after the collection of many more cases is required regarding the FDG uptake of FDCTs and the utility of 18 F-FDG-PET or PET/CT for the differential diagnosis of FDCTs from other splenic lesions. In conclusion, we reported a case of IPT-like FDCT that simultaneously showed delayed enhancement and a capsular-like rim on MR imaging. We suspect that these features are key findings for the differentiation of IPT-like FDCTs from other splenic tumors.
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References 1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
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 1986; 122:562–572. 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 2010; 5:67. Bai LY, Kwang WK, Chiang IP, Chen PM. Follicular dendritic cell tumor of the liver associated with Epstein-Barr virus. Jpn J Clin Oncol 2006; 36:249–253. Cheuk W, Chan JK, Shek TW, et al. Inflammatory pseudotumor-like follicular dendritic cell tumor: a distinctive low-grade malignant intra-abdominal neoplasm with consistent Epstein-Barr virus association. Am J Surg Pathol 2001; 25:721–731. Oz Puyan F, Bilgi S, Unlu E, et al. Inflammatory pseudotumor of the spleen with EBV positivity: report of a case. Eur J Haematol 2004; 72:285–291. Brittig F, Ajtay E, Jaksó P, Kelényi G. Follicular dendritic reticulum cell tumor mimicking inflammatory pseudotumor of the spleen. Pathol Oncol Res 2004; 10:57–60. Fonseca R, Tefferi A, Strickler JG. Follicular dendritic cell sarcoma mimicking diffuse large cell lymphoma: a case report. Am J Hematol 1997; 55:148– 155. Kiryu S, Takeuchi K, Shibahara J, et al. Epstein-Barr virus-positive inflammatory pseudotumour and inflammatory pseudotumour-like follicular dendritic cell tumour. Br J Radiol 2009; 82:e67–e71. Sander B, Middel P, Gunawan B, et al. Follicular dendritic cell sarcoma of the spleen. Hum Pathol 2007; 38:668–672. Takahashi N, Ohya T, Matsumoto H, et al. A case of an inflammatory pseudotumor-like follicular dendritic cell tumor of the spleen unrelated to Epstein-Barr virus. Kita Kanto Igaku 2011; 61:207–214. Tsunemine H, Akasaka H, Kusama T, et al. Hepatic follicular dendritic cell sarcoma favorably controlled by transcatheter arterial chemoembolization. Intern Med 2010; 49:2703–2707. Horiguchi H, Matsui-Horiguchi M, Sakata H, et al. Inflammatory pseudotumor-like follicular dendritic cell tumor of the spleen. Pathol Int 2004; 54:124 – 131. WHO Classification of Tumours of the Haematopoietic and Lymphoid Tissues. Lyon, France: International Agency for Research on Cancer; 2008. Fonseca R, Yamakawa M, Nakamura S, et al. Follicular dendritic cell sarcoma and interdigitating reticulum cell sarcoma: a review. Am J Hematol 1998; 59:161–167. Perez-Ordoñez B, Rosai J. Follicular dendritic cell tumor: review of the entity. Semin Diagn Pathol 1998; 15:144 –154. Ishigami K, Yoshimitsu K, Nishihara Y, et al. Hepatocellular carcinoma with a pseudocapsule on gado-
354
17.
18.
Y. Kitamura et al.
linium-enhanced MR images: correlation with histopathologic findings. Radiology 2009; 250:435–443. Gaetke-Udager K, Wasnik AP, Kaza RK, et al. Multimodality imaging of splenic lesions and the role of non-vascular, image-guided intervention. Abdom Imaging 2014; 39:570–587. Compérat E, Bardier-Dupas A, Camparo P, Capron F, Charlotte F. Splenic metastases: clinicopathologic presentation, differential diagnosis, and pathogene-
19.
20.
sis. Arch Pathol Lab Med 2007; 131:965–969. Abbott RM, Levy AD, Aguilera NS, Gorospe L, Thompson WM. From the archives of the AFIP: primary vascular neoplasms of the spleen: radiologicpathologic correlation. Radiographics 2004; 24: 1137–1163. Metser U, Miller E, Kessler A, et al. Solid splenic masses: evaluation with 18F-FDG PET/CT. J Nucl Med 2005; 46:52–59.
Magnetic Resonance in Medical Sciences
doi:10.2463/mrms.2014-0052
© 2015 Japanese Society for Magnetic Resonance in Medicine
CASE REPORT
Inflammatory Pseudotumor-like Follicular Dendritic Cell Tumor of the Spleen: Case Report and Review of the Literature Yoshiyuki KITAMURA1, Yukihisa TAKAYAMA2, Akihiro NISHIE1*, Yoshiki ASAYAMA1, Yasuhiro USHIJIMA1, Nobuhiro FUJITA1, Koichirou MORITA1, Shingo BABA1, Yuichiro KUBO3, Ken SHIRABE4, and Hiroshi HONDA1 1
Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu University 3–1–1 Maidashi, Higashi-ku, Fukuoka 812–8582, Japan 2 Department of Radiology Informatics and Network, Graduate School of Medical Sciences, Kyushu University 3 Department of Anatomic Pathology, Graduate School of Medical Sciences, Kyushu University 4 Department of Surgery and Science, Graduate School of Medical Sciences, Kyushu University (Received May 1, 2014; Accepted October 29, 2014; published online February 12, 2015)
A 74-year-old woman underwent contrast-enhanced (CE) computed tomography (CT) that revealed an enlarging splenic lesion. This splenic tumor was suspected as metastasis because the patient had been diagnosed with right breast cancer with lung and right axillary lymph node metastases 4 years earlier and had undergone surgery and hormone therapy at another hospital. T 2 -weighted imaging of magnetic resonance (MR) imaging demonstrated the tumor with slightly high intensity with a rim of low intensity at the margin. On dynamic contrast-enhanced (DCE)-MR imaging after intravenous administration of gadolinium diethylenetriamine pentaacetic acid, delayed enhancement was observed in the center and margin of the tumor. On positron emission tomography with 2-deoxy-2-[18F] fluoro-Dglucose (FDG) integrated with CT, the tumor showed high FDG uptake. Splenic metastasis was considered based on the imaging findings, lack of inflammation on laboratory data, and clinical course, so she underwent splenectomy. Histopathologically, the tumor was encapsulated by a fibrous structure, which was depicted as the rim at the tumor margin on T 2 -weighted imaging and DCE-MR imaging. Immunohistochemical study allowed the diagnosis of inflammatory pseudotumor (IPT)-like follicular dendritic cell tumor (FDCT). FDCT is a primary neoplasm of lymph nodes that shows features of follicular dendritic cell differentiation, and it is rare at the spleen. Differential diagnosis is difficult between IPTlike FDCT and similar splenic tumors, such as IPT, splenic metastases, hamartoma and hemangioma. However, in addition to the enhancement pattern within a tumor on DCEMR imaging, detection of the capsular-like rim on MR imaging might aid the diagnosis of splenic IPT-like FDCT. Keywords: Epstein-Barr virus, follicular-dendritic cell tumor (FDCT), MRI, spleen stein-Barr virus (EBV) infection and are referred to as inflammatory pseudotumor (IPT)-like FDCTs because they resemble IPTs histologically. 3–5 Several reports provide imaging findings of splenic FDCTs on computed tomography (CT) and/or magnetic resonance (MR) imaging 6 –12 and describe the lesions as well circumscribed with delayed enhancement. 7,10 These imaging features resemble those of other splenic tumors, such as metastatic tumors, lymphomas, and IPTs, so preoperative diagnosis of FDCTs is difficult. 8 One pathological feature of
Introduction Follicular dendritic cell tumors (FDCTs) are primary neoplasms of the lymph nodes that show features of follicular dendritic cell differentiation. 1 More than 70% of FDCTs occur at the lymph node(s), and 8% of FDCTs occur in the spleen. 2 Splenic FDCTs are generally associated with Ep*Corresponding author, Phone: +81-92-642-5695, Fax: +8192-642-5708, E-mail: [email protected] 347
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FDCTs is the presence of a fibrous capsule between the tumor and the surrounding parenchyma. 4,6 To the best of our knowledge, the presence of capsular formation has rarely been referenced in the differential diagnoses of splenic tumors. The radiological detection of this capsule might be helpful to differentiate splenic IPT-like FDCTs from other splenic tumors. We report a case of a splenic IPT-like FDCT that showed MR findings suggestive of a fibrous capsule, and we discuss the utility of this finding in diagnosing splenic tumors.
Case Report A 74-year-old woman was admitted to our hospital 4 years after she was diagnosed with right breast cancer with lung and right axillary lymph node metastases and underwent surgery and hormone therapy at another hospital. During the course of follow-up after her right mastectomy, contrastenhanced (CE) CT demonstrated a splenic tumor. CE-CT was performed with a 64-row multidetector CT unit (Aquilion 64, Toshiba Medical Systems, Tokyo, Japan) using parameters: 120 kVp, 100 to 300 mAs, 0.5-mm collimation, 0.828 pitch factor, and a single breath-hold helical acquisition of 5 to 8 s, depending on liver size. Using these raw data, transverse images were obtained with a slice thickness of 5 mm and no slice gap. The patient received intravenous administration of a total of 2.0 mL/kg (maximum, 100 mL) of nonionic iodinated contrast agent (Iopamilon 370, 370 mgI/mL, Bayer HealthCare, Osaka, Japan) at a rate of 3.0 mL/s using an automatic injector (Nemoto Kyorindo, Tokyo, Japan). Images scanned 43 s (early phase), 70 s (portal phase) and 240 s (delayed phase) after the beginning of contrast agent administration were used for assessment. The tumor diameter was 15 mm at that time and increased to 29 mm within 10 months. The patient visited our hospital for further evaluation. She had no symptoms. Laboratory tests including complete blood count, blood serum chemistry, and tumor markers (e.g., cancer antigens 15– 3, 19–9, and 125 and C-reactive protein) were within normal limits. The well circumscribed splenic tumor showed similar density to that of the spleen (Fig. 1a) without calcification and inhomogeneous and weak enhancement on early phase image (Fig. 1b). The splenic tumor showed delayed enhancement according to portal- and delayed-phase images (Fig. 1c, d), and the delayed-phase image showed an area of low density within the tumor. She underwent MR imaging for detailed evaluation of the splenic tumor using a 3-tesla MR system. Table 1 details the MR sequence parameters. On in-
Fig. 1. Images of (a) precontrast-enhanced, (b) early, (c) portal, and (d) delayed phases. The early phase was scanned 43 s, portal phase, 70 s, and delayed phase, 240 s after the beginning of contrast agent administration. The well circumscribed splenic tumor showed similar density to the spleen on precontrastenhanced computed tomography (CT) (a) and inhomogeneous and slight enhancement on early-phase image (b). The tumor showed delayed enhancement according to portal- and delayed-phase images (c, d). There was an area of low density within the tumor on delayed-phase image. In this contrast-enhanced (CE) CT image, the tumor diameter was 29 mm.
phase T 1 - (T 1 WI) and fat-suppressed T 2 -weighted imaging (FS-T 2 WI), the signal intensity of the tumor resembled that of the spleen parenchyma (Fig. 2a, b), and a rim of low intensity was depicted at the margin of the tumor (Fig. 2b). On diffusionweighted imaging (DWI) of b-value 1,000 mm2 /s, signal intensity of the tumor was slightly high, but that of the margin of the tumor was low compared with that of the spleen parenchyma (Fig. 2c). The apparent diffusion coefficient (ADC) of the tumor, 0.98 © 10 ¹3 mm 2 /s, was slightly higher than that of the spleen parenchyma, 0.86 © 10¹3 mm2/s (Fig. 2d). On dynamic contrast-enhanced (DCE) MR imaging, signal intensity of the tumor was similar to that of the spleen parenchyma on pre-contrast images (Fig. 3a). After intravenous administration of gadolinium diethylenetriamine pentaacetic acid (GdDTPA, Magnevist, Bayer Healthcare, Osaka, Japan), the tumor showed inhomogeneous and weak enhancement 25 s after contrast introduction (Fig. 3b) and similar enhancement 90 s after contrast introMagnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
Table 1.
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Details of the magnetic resonance (MR) sequence parameters
Parameters
Unit
T1WI (CSI)
ssT2WI
DWI
DCE-MRI
Repetition time Echo time Flip angle Field of view Matrix (frequency © phase) Slice thickness Slice gap Number of slices Number of excitations Fat suppression Respiratory control Band width Scan time of whole slices
(ms) (ms) (degrees) (mm)
160.0 1.15/2.27 60 380 © 329 240 © 207 7.0 1.0 25 1 No Breath-hold 1898.5 00:14.8
1154.0 71.0 90 380 © 299 112 © 88 7.0 1.0 25 1 SPAIR Breath-hold 569.6 00:30.0
1867.0 55.0 90 380 © 299 112 © 88 7.0 1.0 25 1 SPIR Triggered 99.5 01:39.0
3.0 1.4 10 375 © 298 252 © 200 3.0 ¹1.5 133 1 SPAIR Breath-hold
(mm) (mm)
(Hz/pixel) (min:sec)
723.4 17.9
T1WI: T1-weighted imaging, CSI: chemical shift imaging, ssT2WI: single-shot T2-weighted imaging, DWI: diffusionweighted imaging, DCE-MRI: dynamic contrast-enhanced magnetic resonance imaging, SPIR: spectral presaturation with inversion recovery, SPAIR: spectral attenuated with inversion recover
duction (Fig. 3c) compared with the spleen parenchyma. On delayed-phase image obtained 240 s after the administration of Gd-DTPA, the center and margin of the tumor showed enhancement even though other parts of the tumor and the spleen parenchyma showed washout (Fig. 3d). The unenhanced area within the tumor was suspected to represent degenerative change or necrosis. On positron emission tomography with 2-deoxy-2-[18F] fluoro-D-glucose integrated with CT ( 18 F-FDG-PET/CT), the tumor showed high FDG uptake with a maximum standardized uptake value (SUVmax) of 14.3 (Fig. 4). There was no abnormal uptake in any other organ, including the liver, breasts, lungs, and lymph nodes. A malignant tumor including splenic metastasis was considered based on the clinical course, high FDG uptake, and lack of inflammation, so a splenectomy was performed to confirm the diagnosis and clarify a treatment strategy. The tumor measured 36 © 35 mm on gross specimen and histologically comprised a proliferation of lymphocytes, histiocytes, plasma cells, and fibroblastic cells. We also observed many epithelioid cell granulomatous lesions and scattered oval- to spindle-shaped cells with irregular nuclei and identified a fibrous structure between the tumor and the splenic parenchyma (Fig. 5a). Immunohistochemically, the infiltrating oval- to spindle-shaped cells were positive for fascin but negative for CD21, CD35, anaplastic lymphoma kinase (ALK), Epstein-Barr virus latent membrane protein (EBV-LMP), and Epstein- Barr virus nuclear antigen antibody (EBNA). EpsteinBarr virus-encoded small RNA (EBV-EBER) was Vol. 14 No. 4, 2015
positive by in situ hybridization (Fig. 5b). Although FDC markers were negative, these histological features suggested IPT-like FDCT. Two years after the splenectomy, the patient was alive and showed no evidence of recurrent disease.
Discussion FDCT is a rare neoplasm classified as a histiocytic and dendritic neoplasm. 13 Monda and associates reported this tumor first in 1986 as a primary neoplasm of lymph nodes that showed features of follicular dendritic cell (FDC) differentiation. 1 A malignant proliferation of FDCT is called a follicular dendritic cell sarcoma. 14 FDCs normally act as antigen-presenting cells for B cells and promote Bcell proliferation and differentiation. 14 FDCTs are thought to occur mainly at lymph nodes, most commonly in the cervical and axillary regions. 15 The tumor may also occur at various extranodal sites, such as the palate, pharynx, tonsil, thyroid, mediastinum, gastrointestinal tract, liver, and spleen as a slow-growing, well circumscribed, and painless mass. 2 The symptoms of FDCTs, such as low grade fever, weight loss, epigastralgia, abdominal fullness, and slight anemia, are nonspecific. The diagnosis of FDCT is usually made by histological examination. Histologically, FDCTs are characterized by the syncytial growth of spindle or ovoid cells, which are immunoreactive for such various FDC markers as CD21 and CD35. 4 A storiform or whorled growth pattern is frequently encountered. 3
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Fig. 2. (a) In-phase T1-weighted imaging (T1WI), (b) fat-suppressed T2-weighted imaging (FS-T2WI), (c) diffusion-weighted imaging (DWI) of b-value with 1,000 mm2/s, and (d) apparent diffusion coefficient (ADC) map of magnetic resonance (MR) imaging. The signal intensity of the splenic tumor was similar to that of the spleen parenchyma on T1WI and FST2WI (a, b). The tumor showed slightly higher signal intensity than the spleen parenchyma on DWI. The tumor demonstrated a rim of low intensity on FST2WI and DWI (b, c). The ADC value of the tumor, 0.98 © 10¹3 mm2/s, was slightly higher than that of the spleen parenchyma, 0.86 © 10¹3 mm2/s (d).
Fig. 3. Dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) (a) pre-enhancement and (b) 25, (c) 90, and (d) 240 s after the administration of gadolinium diethylenetriamine pentaacetic acid (GdDTPA). Signal intensity of the splenic tumor was similar to that of the spleen parenchyma on pre-contrast images (a). The tumor showed inhomogeneous and weak enhancement (b) and similar enhancement (c) compared with that of the spleen parenchyma. The tumor showed delayed enhancement at the center and margin of the tumor (d). Delayed enhancement at the margin of the tumor was considered the rim (d). The unenhanced area within the tumor was suspected to represent degenerative change or necrosis (d).
FDCTs are categorized into 2 types–conventional FDCTs composed of the storiform, fascicular, and diffuse growth of tumor cells with a sprinkling of lymphocytes and IPT-like FDCTs composed of dispersed tumor cells with intense lymphocytes and plasma cells. 4 EBV-positive IPT is sometimes used instead of IPT-like FDCT to refer to this entity, but EBV-positive IPT and IPT-like FDCT may be considered the same disease entity, although more discussion is required. 8 Most FDCTs arising at the liver or spleen are categorized as IPT-like FDCTs, and this type is rare at other sites. 4 IPT-like FDCTs arising at the liver or spleen are associated with EBV infection, whereas conventional FDC tumors show EBV association in only one of 25 cases (4%). 3–5 Thus, the identification of EBV infection is important in the diagnosis of IPT-like FDCTs by immunostaining for EBV-LMP, which is a protein product
of EBV with transforming function, or by the detection of the EBER gene by in situ hybridization. 4 Other clinicopathologic features of IPT-like FDCT that differ from those of conventional FDCT include female predilection, occurrence in intra-abdominal sites, systemic inflammatory symptoms such as weight loss and fever, indolent clinical course such as less frequent recurrence, and metastasis. 4 Complete surgical resection is the first choice to treat IPT-like FDCTs because they are thought to have a low-to-intermediate malignancy potential despite an indolent clinical course. 4 Systemic chemotherapy and radiotherapy have also been used as treatment methods, but their efficacy in improving patients’ survival rate is not established. A long follow-up is also necessary for IPT-like FDCTs after treatment. 4 Only 19 cases of splenic IPT-like FDCTs or IPTs Magnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
with EBV positivity have been reported. 2,4,6 –12 Ten of 19 cases have been described their imaging findings (Table 2). 6–12 Of them, CT findings were described in 8 cases, all of which showed a well circumscribed margin. CE-CT in 7 cases showed heterogeneous enhancement. 7,8,10 –12 MR imaging was performed in 2 cases. 8,10 Tumors in the previous reports showed isointensity on T 1 WI, low intensity on T 2 WI, and homogenous or heterogeneous delayed enhancement on DCE-MR imaging. The T 1 WI and DCE-MR imaging findings for our patient were consistent with those reported previously. 8,10 Delayed enhancement of an IPT-like FDCT on CE-CT and DCE-MR imaging is a satisfactory finding because of its similar histology with that of IPT. However, our patient’s tumor showed slightly high signal intensity on T 2 WI, which was inconsistent with the signal intensity of the previous cases. IPTs show variable signal intensity on T 2 WI according to their constituent contents. 5 This difference in T 2 signal intensity may be due to the amount of inflammatory and/or spindle fibrosis within each tumor. Our patient’s T 2 WI depicted a rim of low intensity at the margin of the tumor. This rim was also shown with delayed enhancement on DCE-MR imaging. In the comparison with the histological
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Fig. 4. Fusion image of positron emission tomography with 2-deoxy-2-[18F] fluoro-D-glucose integrated with computed tomography ( 18F-FDG-PET/CT). The splenic tumor showed high FDG uptake with a maximum standardized uptake value (SUVmax) of 14.3.
Fig. 5. (a) Macroscopic and (b) microscopic graphs of the specimen from the spleen. Microscopic graph (hematoxylin and eosin stain ©40) showed that the tumor (T) comprised a proliferation of lymphocytes, histiocytes, plasma cells, and fibroblastic cells accompanied by many epithelioid cell granulomatous lesions and scattered oval- to spindleshaped cells with irregular nuclei. A fibrous structure (arrows) was identified between the tumor (T) and the splenic parenchyma. (c) FS-T2WI of the spleen (same image as Fig. 2b). (d) Epstein-Barr virus-encoded small RNA (EBVEBER) was positive by in situ hybridization (©400). Vol. 14 No. 4, 2015
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Table 2.
Summary of the reported cases of splenic follicular dendritic cell tumor (FDCT) including imaging findings Tumor size (cm)
Case No.
Age (yrs)/ Sex
1
54/M
2
64/M
n/a
3
56/F
4
4
60/M
2
5
78/F
3
6 7
44/F 39/M
11 © 8 8
8
78/F
7 © 7.5
9
77/F
10
74/F
Findings of computed tomography (CT)*
12 © 17 Low attenuation on CT (images not available) Heterogeneous weak enhancement on contrastenhanced (CE) CT Heterogeneous weak enhancement on CE-CT
Heterogeneous weak enhancement on CE-CT Heterogeneous weak enhancement on CE-CT Cystic tumor Heterogeneous delayed enhancement on CE-CT
Heterogeneous enhancement on CE-CT 11 © 9©9 Heterogeneous enhancement with area of low density at the center of the tumor on CE-CT 3.6 © 3.5 Heterogeneous delayed enhancement with area of low density within the tumor on CE-CT
Findings of magnetic resonance imaging (MRI)*
Histopathological findings of the capsular-like rim
n/a
Surrounded by fibrous tissue with a low number of fibroblasts n/a
n/a
Our review of the imaging Ref. findings of the capsular-like rim n/a
(6)
Nonidentifiable
(7)
Iso-signal intensity on T1WI, low signal intensity on T2WI, and delayed enhancement on DCE-MRI n/a
n/a
Identifiable on T2WI
(8)
n/a
Nonidentifiable
(8)
n/a
n/a
Nonidentifiable
(8)
n/a n/a Marked low signal n/a intensity on T1WI and T2WI and delayed enhancement on DCE-MRI n/a n/a
Nonidentifiable Nonidentifiable
(9) (10)
Nonidentifiable
(11)
n/a
n/a
Nonidentifiable
(12)
Iso-signal intensity on T1WI and T2WI and delayed enhancement on DCE-MRI
Fibrous structure at part of the tumor circumference
Identifiable on T2WI and DCE-MRI
Our case
*Attenuations at CE-CT and signal intensities at MRI of the splenic FDCTs are compared with those of the spleen parenchyma. n/a, not available; DCE-MRI, dynamic contrast-enhanced MRI; Ref., reference number; T1WI, T1-weighted imaging; T2WI, T2-weighted imaging
findings, a fibrous structure demarcated the tumor from the spleen parenchyma. This fibrous structure would probably be demonstrated as an imaging finding. The previous reports seem to describe the capsular-like rim at the margin of IPT-like FDCTs, although the authors do not mention it specifically. 8,10 In our case, difficult depiction of the capsu-
lar-like rim on CE-CT was possibly related to low contrast between lesion and nonlesion between the capsular-like rim and spleen parenchyma. Thus, MR imaging is more advantageous than CT for evaluating the capsular-like rim at the margin of IPT-like FDCT. Histologically, it is known that IPT-like FDCTs Magnetic Resonance in Medical Sciences
Findings of Splenic IPT-like FDCT
occasionally show a peritumoral fibrous capsule. These tumors are well circumscribed and show expansive growth. 6 The frequency of a capsular-like rim of the splenic IPT-like FDCT is unknown. We could evaluate the capsular-like rim of a splenic IPT-like FDCT in only one previous report, but the authors did not discuss it. 6 Our report is the first to mention imaging findings of this capsular-like rim. The peritumoral fibrous capsule might be the secondary product of an interaction between the tumor and the host spleen, which might be the similar interaction between a hepatocellular carcinoma and the host liver. 16 A tumor showing delayed enhancement and a capsular-like rim simultaneously would be extremely rare. Splenic metastases show usually minimal to heterogeneous centripetal enhancement that depends on the primary neoplasm. 17 Pathological findings of splenic metastases have also been reported. 18 However, we found no report concerning the peritumoral fibrous capsule of splenic metastases. The radiological detection of this capsule might be helpful to differentiate splenic IPT-like FDCTs from other splenic tumors, although more discussion is required to clarify the clinical utility of the finding. Other important differential diagnoses of splenic tumors that show delayed enhancement are hamartoma and hemangioma. These tumors do not show the capsular-like rim because their growth is very slow, so the peritumoral fibrous capsule rarely occurs. 19 Therefore, the combination of delayed enhancement and a capsular-like rim may be imaging findings that help us differentiate IPT-like FDCTs from other splenic tumors. Only one case report described 18 F-FDG-PET/ CT findings of a follicular dendritic cell sarcoma, but not FDCT. In that report, the tumor showed high FDG uptake. 11 Our patient’s IPT-like FDCT also showed high FDG uptake, but 18 F-FDG-PET or PET/CT may not be helpful for the differentiation of IPT-like FDCT from other splenic tumors because some splenic tumors, such as metastatic tumors or lymphomas, can also show high FDG uptake. 20 Further evaluation after the collection of many more cases is required regarding the FDG uptake of FDCTs and the utility of 18 F-FDG-PET or PET/CT for the differential diagnosis of FDCTs from other splenic lesions. In conclusion, we reported a case of IPT-like FDCT that simultaneously showed delayed enhancement and a capsular-like rim on MR imaging. We suspect that these features are key findings for the differentiation of IPT-like FDCTs from other splenic tumors.
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References 1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
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 1986; 122:562–572. 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 2010; 5:67. Bai LY, Kwang WK, Chiang IP, Chen PM. Follicular dendritic cell tumor of the liver associated with Epstein-Barr virus. Jpn J Clin Oncol 2006; 36:249–253. Cheuk W, Chan JK, Shek TW, et al. Inflammatory pseudotumor-like follicular dendritic cell tumor: a distinctive low-grade malignant intra-abdominal neoplasm with consistent Epstein-Barr virus association. Am J Surg Pathol 2001; 25:721–731. Oz Puyan F, Bilgi S, Unlu E, et al. Inflammatory pseudotumor of the spleen with EBV positivity: report of a case. Eur J Haematol 2004; 72:285–291. Brittig F, Ajtay E, Jaksó P, Kelényi G. Follicular dendritic reticulum cell tumor mimicking inflammatory pseudotumor of the spleen. Pathol Oncol Res 2004; 10:57–60. Fonseca R, Tefferi A, Strickler JG. Follicular dendritic cell sarcoma mimicking diffuse large cell lymphoma: a case report. Am J Hematol 1997; 55:148– 155. Kiryu S, Takeuchi K, Shibahara J, et al. Epstein-Barr virus-positive inflammatory pseudotumour and inflammatory pseudotumour-like follicular dendritic cell tumour. Br J Radiol 2009; 82:e67–e71. Sander B, Middel P, Gunawan B, et al. Follicular dendritic cell sarcoma of the spleen. Hum Pathol 2007; 38:668–672. Takahashi N, Ohya T, Matsumoto H, et al. A case of an inflammatory pseudotumor-like follicular dendritic cell tumor of the spleen unrelated to Epstein-Barr virus. Kita Kanto Igaku 2011; 61:207–214. Tsunemine H, Akasaka H, Kusama T, et al. Hepatic follicular dendritic cell sarcoma favorably controlled by transcatheter arterial chemoembolization. Intern Med 2010; 49:2703–2707. Horiguchi H, Matsui-Horiguchi M, Sakata H, et al. Inflammatory pseudotumor-like follicular dendritic cell tumor of the spleen. Pathol Int 2004; 54:124 – 131. WHO Classification of Tumours of the Haematopoietic and Lymphoid Tissues. Lyon, France: International Agency for Research on Cancer; 2008. Fonseca R, Yamakawa M, Nakamura S, et al. Follicular dendritic cell sarcoma and interdigitating reticulum cell sarcoma: a review. Am J Hematol 1998; 59:161–167. Perez-Ordoñez B, Rosai J. Follicular dendritic cell tumor: review of the entity. Semin Diagn Pathol 1998; 15:144 –154. Ishigami K, Yoshimitsu K, Nishihara Y, et al. Hepatocellular carcinoma with a pseudocapsule on gado-
354
17.
18.
Y. Kitamura et al.
linium-enhanced MR images: correlation with histopathologic findings. Radiology 2009; 250:435–443. Gaetke-Udager K, Wasnik AP, Kaza RK, et al. Multimodality imaging of splenic lesions and the role of non-vascular, image-guided intervention. Abdom Imaging 2014; 39:570–587. Compérat E, Bardier-Dupas A, Camparo P, Capron F, Charlotte F. Splenic metastases: clinicopathologic presentation, differential diagnosis, and pathogene-
19.
20.
sis. Arch Pathol Lab Med 2007; 131:965–969. Abbott RM, Levy AD, Aguilera NS, Gorospe L, Thompson WM. From the archives of the AFIP: primary vascular neoplasms of the spleen: radiologicpathologic correlation. Radiographics 2004; 24: 1137–1163. Metser U, Miller E, Kessler A, et al. Solid splenic masses: evaluation with 18F-FDG PET/CT. J Nucl Med 2005; 46:52–59.
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