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1 Surgical Pathology Companion Meeting Case 5: Locally Recurrent Chest wall Mass Cristina Antonescu, MD Department of Pathology, Memorial Sloan Kettering Cancer Center Disclosure of Relevant Financial Relationships The USCAP requires that anyone in a position to influence or control the content of all CME activities disclose any relevant relationship(s) which they or their spouse/partner have, or have had within the past 12 months with a commercial interest(s) [or the products or services of a commercial interest] that relate to the content of this educational activity and create a conflict of interest. Complete disclosure information is maintained in the USCAP office and has been reviewed by the CME Advisory Committee. No conflict of interest to disclose. Case History CT Local Recurrence in the resection bed 41 year old man who underwent a right chest wall mass en bloc resection for a lesion involving the 3 rd rib. The tumor was diagnosed as a low grade malignant tumor at the outside hospital, and appeared completely excised. The patient presented 4 years later at our Institution for a local recurrence in the soft tissue chest wall bed, for which a re excision was performed. Frozen tissue for molecular characterization was made available at the time. 1
2 Low Power: Nodular Growth Pattern High Power: solid growth in a hemorrhagic background Epithelioid cells with dense eosinophilic cytoplasm Intra cytoplasmic empty vacuoles (so called blister cells ) Overt vasoformation dilated lumens Overt vasoformation small vessels Plump endothelial cells with eccentric, bulging nuclei tombstone pattern Periphery of the lesion 2
3 Epithelioid Vascular Neoplasm? Atypical histologic features Differential Diagnosis Present Solid growth Increased cellularity Mild nuclear pleomorphism Mitotic Activity Absent Necrosis Marked Pleomorphism Atypical mitoses Epithelioid Hemangioma Epithelioid Hemangioendothelioma Lacks well formed channels Molecular: WWTR1 CAMTA1 Epithelioid Angiosarcoma High nuclear grade, macronucleoli, necrosis RNA Sequencing Discovery RT PCR Experimental Validation both transcripts FISH 3
4 Epithelioid Hemangioma (EH) Diagnosis: Epithelioid Hemangioma of Bone with FOS LMNA Fusion Definition Benign vasoformative tumor composed of epithelioid/histiocytoid endothelial cells Morphologic spectrum wide solid growth, mature vessels, blister cells variable inflammatory infiltrate (lymphocytes, eosinophils) Clinical Features Wide age range (peak 3 rd 5 th decade) Location: head & neck, soft tissue & bone of extremities, penis Epithelioid Hemangioma Pathologic Features Vasoformation lined by hobnailed epithelioid cells, tombstone pattern Epithelioid Hemangioma Pathologic Features Well formed, mature vessels Lobular growth pattern R distal femur, 35yM Recurrent Rib mass 4
5 Epithelioid Hemangioma Worrisome Histologic Features Angiolymphoid Hyperplasia with Eosinophilia Synonymous to Epithelioid Hemangioma Rosai J, Arch Dermatol 1974; Castro C, Cancer 1974 Solid growth pattern Nuclear enlargement Mild nuclear pleomorphism Scattered mitotic figures? True neoplastic vs reactive process angiocentric distribution Inflammation mural damage overlap with Kimura disease Fetsch JF, Weiss SW. Observations concerning the pathogenesis of epithelioid hemangioma (angiolymphoid hyperplasia). Mod Pathol 1991 Angiolymphoid Hyperplasia with Eosinophilia (ALHE) Genetics of Epithelioid Hemangioma mostly skin/h&n mixed lymph and eos inflammatory infiltrate vascular damage blow out pattern Fibro intimal hyperplasia Angiocentric capillary proliferation Medium sized muscular vessel wall FOS gene rearrangements in 30% of EH with different gene partners (LMNA, Vimentin) (Huang SC, AJSP 2015; van IJzendoorn DG, Genes Chromosome Cancer 2015) ZFP36 FOSB fusions in 20% of EH showing atypical histology (Antonescu CR, Genes Chromosome Cancer 2014) 5
6 Epithelioid Hemangioma with FOS Gene Rearrangements: 17/58 (29%) Epithelioid Hemangioma with FOS Gene Rearrangements Mean age: 43 years (range 15 67) Male gender (12 M/5 F) Location: Extremities: 71% Trunk: 18% Head and neck: 6% Penis: 6% Huang SC et al, Am J Surg Pathol 2015 Tissue Planes: Bone: 59% Soft tissue: 35% Cutaneous: 6% (penile) Histologic variants: Cellular variant: 71% Typical variant: 29% ALHE: 0% Huang SC et al, Am J Surg Pathol 2015 FOS rearranged Typical EH 23/M, 9 th rib FOS positive Cellular EH Solid growth Radiographic findings were suggestive of fibrous dysplasia Low power lobulated pattern Well formed vascular spaces Intra vascular growth Spindling 6
7 FOS rearranged EH with unusual histologic features No FOS gene rearrangements in Angiolymphoid Hyperplasia with Eosinophilia Infiltrative pattern, penis Marked inflammation, bone FISH negative in all 12 cases FOS gene fusion partner FISH positional cloning identified VIM (vimentin) gene as FOS partner LMNA was only found in the index case and not found in any other FOS rearranged EH Review of the literature for other epithelioid vascular tumors involving the FOS gene locus at 14q24 A previous intra osseous EHE reported as 46, XX, 6, t(10;14)(p13;q24) karyotype He M et al, Cancer Genet Cytogenet 2006 t(10;14)(p13;q24) VIM Break apart FISH assay He M et al, Cancer Genet Cytogenet
8 FOS VIM positive Bone Epithelioid Hemangioma FOS VIM positive Bone Epithelioid Hemangioma 56/F multifocal, foot cellular variant NED 9 years FOS VIM positive Bone Epithelioid Hemangioma 38/F solitary bone lesion, cuboid cellular variant NED 2 years Epithelioid Hemangioma with FOSB gene alterations (ZFP36 FOSB fusions) EH with atypical Histologic Features 8
9 Index Case Proximal Tibia 52/M necrosis Antonescu CR, Genes Chromosome Cancer 2014 ZFP36 FOSB positive Epithelioid Hemangioma N=9/46 (20%) 8M/1F; mean age 37 yrs (11 51) Location: Penis, n=4 bone, soft tissue Atypical histologic features: Mild to moderate pleomorphism Necrosis (n=3) No recurrences to date (FU limited) ZFP36 FOSB positive 4/6 Penile Epithelioid Hemangioma 27/M 51/M Antonescu CR, Genes Chromosome Cancer
10 ZFP36 FOSB positive Soft Tissue Epithelioid Hemangioma Epithelioid Hemangioma of Bone Controversy Multifocal presentation/destructive growth Aggressive radiographic appearance Rare lymph node involvement Limited eosinophilic infiltrate Worrisome histologic features Indistinguishable from hemangioendothelioma of bone Is different from angiolymphoid hyperplasia with eosinophilia of skin and soft tissue Behavior from benign to low grade malignant Aggressive Radiographic Findings and Multifocality in Epithelioid Hemangioma of Bone FOS & FOSB Gene Rearrangements in EH of Bone in 75 85% Distinct from the genetic abnormalities seen in Epithelioid Hemangioendothelioma FOS gene rearrangements: 59% (10/17) Huang et al, Amer J Surg Pathol % (5/7) van IJzendoorn DG, Genes Chromosome Cancer 2015 A radiograph of the 1 st metatarsal replaced and expanded by a multiseptated lytic lesion. axial T2 MR image with tumor deposits as areas of bright signal in several bones of foot A sagittal MR image shows multinodular tumor deposits in the arm FOSB gene rearrangements: 14% (2/14) Antonescu CR et al, Amer J Surg Pathol 2014 Both with necrosis Calcaneus (multifocal: foot ankle) 10
11 FOS gene family FBJ murine osteosarcoma viral oncogene homolog Fos family: FOS, FOSB, FOSL1, and FOSL2. No FOSL1 or FOSL2 gene rearrangement in other EHs Encode leucine zipper proteins that can dimerize with proteins of the JUN family, thereby forming the transcription factor complex AP 1. Implicated as regulators of cell proliferation, differentiation, and transformation Marconcini, Proc Natl Acad Sci U S A The other vascular tumor with FOSB gene rearrangements Epithelioid Sarcoma like Hemangioendothelioma (Billings SD et al. Am J Surg Pathol 2003) Pseudomyogenic Hemangioendothelioma (Hornick JL et al. Am J Surg Pathol 2011) Epithelioid Sarcoma like Hemangioendothelioma Pseudomyogenic Hemangioendothelioma rhabdomyoblast like appearance brightly eosinophilic cytoplasm resemble Epithelioid Sarcoma more than EHE morphologically express epithelial and vascular markers such as CD31, Fli1 young adults, limbs, multifocal, rare locoregional metastases Billings et al; Am J Surg Pathol 2003 Young males, multifocal, high local recurrence Diffuse positivity for AE1:AE3 and Fli1, variable for CD31 Hornick et al. Amer J Surg Pathol
12 Pseudomyogenic Hemangioendothelioma Pseudomyogenic Hemangioendothelioma Recurrent SERPINE1 FOSB Gene Fusions (Walther C, J Pathol 2014) FISH analysis showing FOSB and SERPINE1 Gene Rearrangements FOSB SERPINE1 CD31 ERG 30/M FOS gene family abnormalities in vascular tumors FOS rearrangements in 30% of EH (up to 70% in bone EH) ZFP36 FOSB in 20% of EH (+/ atypical histologic features; higher in penile site) SERPINE1 FOSB predominant gene fusion in pseudomyogenic (epithelioid sarcoma like) hemangioendothelioma Differential Diagnosis Epithelioid Vascular Tumors Epithelioid Hemangioma (benign) Pseudomyogenic Hemangioendothelioma (a.k.a. Epithelioid sarcoma like Hemangioendothelioma) (rarely metastasizing category) Epithelioid Hemangioendothelioma (malignant) Epithelioid Angiosarcoma (malignant) 12
13 Epithelioid Hemangioendothelioma Epithelioid Hemangioendothelioma Pathology epithelioid endothelial cells arranged in cords, nests angiocentric malignant vascular tumor superficial or deep ST limbs painful 3 rd decade of life, slight female predominance Epithelioid Hemangioendothelioma Pathology Immature Intra cytoplasmic lumina blisters cells Epithelioid Hemangioendothelioma Pathology A distinctive stroma of sulphated acid rich matrix: myxochondroid, hyaline, myxoid 13
14 Epithelioid Hemangioendothelioma Pathology Growth Pattern: cords, single file solid diffuse infiltrative (not lobular) A A 1 t(1;3)(p36.3;q24) 3 Mendlick M et al. AJSP 2001 Consistent WWTR1 CAMTA1 Fusions in EHE Positional Cloning by FISH (Errani C, Genes Chr Cancer 2011) RNAseq Illumina platform & FusionSeq (Tanas MR, Science Translational Medicine 2011) No mature vascular channel formation! WWTR1 CAMTA1 fused signals by FISH RT PCR validation Unusual EHE Subset with alveolar pattern EHE Subset with TFE3 gene rearrangements WWTR1 CAMTA1 negative IHC: strong TFE3 expression as well as endothelial markers (but negative for CK and HMB45) TFE3 FISH: TFE3 gene rearrangements TFE3 30/F, popliteal mass, metastatic to liver CD31 Red, centromeric; Green, telomeric 14
15 EHE Subset with TFE3 gene rearrangements EHE Subset with TFE3 gene rearrangements ERG TFE3 50yM, T2 vertebra 35/M, H&N soft tissue, multiple LR and loco reg mets, NED 22 yrs FU EHE Subset with TFE3 gene rearrangements Recurrent YAP1 TFE3 Fusion in a subset of EHE YAP1 11q22.1 Multifocal Pulmonary Involvement TFE3 Xp11.22 TFE3 TFE3 YAP1 Rhomboid crystals Antonescu CR, Genes Chr Cancer
16 YAP1 TFE3 Fusion Positive EHE (n=10) High Grade Epithelioid Angiosarcoma Young adults, mean 30 yrs old Location: ST, bone, lung Epithelioid cells with abundant eosinophilic cytoplasm Well formed vascular spaces (pseudo alveolar) Indolent clinical course, despite high propensity for metastases Screened by TFE3 IHC/FISH To be determined if YAP1 TFE3 positive EHE will be classified under EHE or a separate entity Antonescu CR, Genes Chr Cancer 2013 Differential Diagnosis of Epithelioid Vascular Tumors WWTR1 CAMTA1 TFE3 Conclusions EHE : soft tissue arm FOS, FOSB EHE: soft tissue arm FOS and FOSB gene rearrangements are present in more than half of EH, especially in cellular and atypical variants. FISH analysis can be used in challenging cases to distinguish from EHE and epithelioid AS Dysregulation of the FOS family of transcription factors through chromosomal translocation is a key event in the tumorigenesis of EH. The lack of FOS gene abnormalities in the ALHE variant suggest a different pathogenesis EH: penis HG epithelioid AS : FISH ( ) 16
17 Conclusions EH of bone harbor FOS and FOSB gene rearrangements in 75 85% of cases, distinct from the genetics of EHE Molecular findings finally confirm that EH in the bone is a standalone pathologic entity Despite some atypical histologic features, locally aggressive behavior or occasional multifocal growth the accumulating clinical evidence is in keeping with a BENIGN neoplasm Morphologic Spectrum Index case Epithelioid Hemangioma with ZFP36 FOSB Gene Fusions Hemorrhagic background Antonescu CR, Genes Chromosome Cancer
18 Differential Diagnosis Epithelioid hemangioendothelioma (EHE) Angiocentric, cords of epithelioid endothelial cells in myxohyaline stroma WWTR1 CAMTA1, YAP1 TFE3 fusions Epithelioid angiosarcoma (AS) Solid proliferation or inter anastomotic channels of highly pleomorphic epithelioid endothelial cells KDR, PTPRB, PLCG1, mutations or MYC/FLT4 gene amplification 18
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