Chondroid Synoviocytic Neoplasm: A Clinicopathologic, Immunohistochemical, and Molecular Genetic Study of a Distinctive Tumor of Synoviocytes

Erica Y Kao; Fisun Ardic; Numrah Fadra; Jessica D Hohenstein; Rohini Mopuri; Doris E Wenger; Lukas Streich; Lisa M Hines; Andrew L Folpe

doi:10.1016/j.modpat.2024.100598

Chondroid Synoviocytic Neoplasm: A Clinicopathologic, Immunohistochemical, and Molecular Genetic Study of a Distinctive Tumor of Synoviocytes

Mod Pathol. 2024 Aug 23;37(11):100598. doi: 10.1016/j.modpat.2024.100598. Online ahead of print.

Authors

Erica Y Kao¹, Fisun Ardic², Numrah Fadra³, Jessica D Hohenstein³, Rohini Mopuri³, Doris E Wenger⁴, Lukas Streich⁵, Lisa M Hines⁶, Andrew L Folpe⁷

Affiliations

¹ Department of Pathology, Brooke Army Medical Center, San Antonio, Texas.
² University of Health Sciences, Dr AY Ankara Oncology Training and Research Hospital, Ankara, Turkey.
³ Division of Computational Biology, Department of Quantitative Health Sciences Research, Mayo Clinic, Rochester, Minnesota.
⁴ Department of Radiology, Mayo Clinic, Rochester, Minnesota.
⁵ Department of Pathology, Oregon Health Sciences University, Portland, Oregon.
⁶ Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, Minnesota.
⁷ Department of Pathology and Laboratory Medicine, Mayo Clinic, Rochester, Minnesota. Electronic address: folpe.andrew@mayo.edu.

PMID: 39181450
DOI: 10.1016/j.modpat.2024.100598

Abstract

Tumors resembling tenosynovial giant cell tumor (TGCT) but additionally forming chondroid matrix are rare and most often involve the temporomandibular joint (TMJ). We studied 21 tumors consisting of synoviocytes (large, eosinophilic mononuclear cells containing hemosiderin) and chondroid matrix to better understand these unusual neoplasms. The tumors occurred in 10 males and 11 females, in the age group of 31 to 80 years (median, 50 years) and involved the TMJ region (16), extremities (4), and spine (1). As in conventional TGCT, all were composed of synoviocytes, small histiocytes, foamy macrophages, siderophages, and osteoclast-like giant cells in variably hyalinized background. Expansile nodules of large, moderately atypical synoviocytes were present, in addition to "chondroblastoma-like," "chondroma-like," or "phosphaturic mesenchymal tumor-like" calcified matrix. The synoviocytes expressed clusterin (17/19) and less often desmin (3/15). The tumors were frequently CSF1 positive by chromogenic in situ hybridization (8/13) but at best weakly positive for CSF1 by immunohistochemistry (0/3). Background small histiocytes were CD163 positive (12/12). All were FGF23 negative (0/10). Cells within lacunae showed a synoviocytic phenotype (clusterin positive; S100 protein and ERG negative). RNA-Seq was successful in 13 cases; fusions were present in 7 tumors, including FN1::TEK (5 cases); FN1::PRG4 (2 cases); and MALAT1::FN1, PDGFRA::USP35, and TIMP3::ZCCHC7 (1 case each). Three tumors contained more than 1 fusion (FN1::PRG4 with TIMP3::ZCCHC7, FN1::TEK with FN1::PRG4, and FN1::TEK with MALAT1::FN1). Clinical follow-up (17 patients; median follow-up duration 38 months; range 4-173 months) showed 13 (76%) to be alive without evidence of disease and 4 (24%) to be alive with persistent/recurrent local disease. No metastases or deaths from disease were observed. We conclude that these unusual tumors represent a distinct category of synoviocytic neoplasia, which we term "chondroid synoviocytic neoplasm," rather than simply ordinary TGCT with cartilage. Despite potentially worrisome morphologic features, they appear to behave in at most a locally aggressive fashion.

Keywords: CSF1; FGF23; FN1; calcified chondroid mesenchymal neoplasm; chondroid synoviocytic neoplasm; immunohistochemistry; molecular genetics; pigmented villonodular synovitis; tenosynovial giant cell tumor.