Malignant gastrointestinal neuroectodermal tumor: clinicopathologic, immunohistochemical, ultrastructural, and molecular analysis of 16 cases with a reappraisal of clear cell sarcoma-like tumors of the gastrointestinal tract

Am J Surg Pathol. 2012 Jun;36(6):857-68. doi: 10.1097/PAS.0b013e31824644ac.

Abstract

The clinical, histologic, immunophenotypic, ultrastructural, and molecular features of a distinctive gastrointestinal tumor are described. Sixteen patients, 8 women and 8 men aged 17 to 77 years (mean age, 42 y; 63% less than 40 y) presented with abdominal pain, intestinal obstruction, and an abdominal mass. Mean tumor size was 5.2 cm (range, 2.4 to 15.0 cm). The tumors arose in the small bowel (10), stomach (4), and colon (2) and were histologically characterized by a sheet-like or nested population of epithelioid or oval-to-spindle cells with small nucleoli and scattered mitoses. Five cases showed focal clearing of the cytoplasm. Scattered osteoclast-type multinucleated giant cells were present in 8 cases. The tumor cells were positive for S-100 protein, SOX10, and vimentin in 100% of cases, for CD56 in 70%, for synaptophysin in 56%, for NB84 in 50%, for NSE in 45%, and for neurofilament protein in 14% of cases. All cases tested were negative for specific melanocytic, gastrointestinal stromal tumors, epithelial, and myoid markers. Ultrastructural examination of 5 cases showed features of primitive neuroectodermal cells with clear secretory vesicles, dense-core granules, occasional gap junctions, and no evidence of melanogenesis. EWSR1 gene rearrangement was assessed by fluorescence in situ hybridization in 14 cases. Twelve cases (86%) showed split EWSR1 signal consistent with a chromosomal translocation involving EWSR1. One case showed extra intact signals, indicating that the nuclei possessed either extra copies of the EWSR1 gene or chromosome 22 polysomy. Only 1 case showed no involvement of the EWSR1 gene. Six cases demonstrated rearrangement of the partner fusion gene ATF1 (46%), and 3 showed rearrangement of CREB1 (23%); 2 cases lacked rearrangement of either partner gene. Clinical follow-up was available in 12 patients and ranged from 1.5 to 106 months. Six patients died of their tumors (mean survival, 32 mo; 83% less than 24 mo). At last follow-up, 4 patients were alive with regional, lymph node, and liver metastases, and 2 patients were alive with no evidence of disease. The tumor described here is an aggressive form of neuroectodermal tumor that should be separated from other primitive epithelioid and spindle cell tumors of the gastrointestinal tract. The distinctive ultrastructural features and absence of melanocytic differentiation serve to separate them from soft tissue clear cell sarcomas involving the gastrointestinal tract. The designation "malignant gastrointestinal neuroectodermal tumor" is proposed for this tumor type.

Publication types

  • Case Reports
  • Multicenter Study

MeSH terms

  • Activating Transcription Factor 1 / genetics
  • Activating Transcription Factor 1 / metabolism
  • Adolescent
  • Adult
  • Aged
  • Biomarkers, Tumor / metabolism
  • Calmodulin-Binding Proteins / genetics
  • Calmodulin-Binding Proteins / metabolism
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Cytoplasmic Granules / metabolism
  • Cytoplasmic Granules / ultrastructure
  • Female
  • Gastrointestinal Neoplasms / genetics
  • Gastrointestinal Neoplasms / metabolism
  • Gastrointestinal Neoplasms / mortality
  • Gastrointestinal Neoplasms / pathology*
  • Gene Fusion
  • Gene Rearrangement
  • Humans
  • In Situ Hybridization, Fluorescence
  • Male
  • Middle Aged
  • Neuroectodermal Tumors, Primitive, Peripheral / genetics
  • Neuroectodermal Tumors, Primitive, Peripheral / metabolism
  • Neuroectodermal Tumors, Primitive, Peripheral / mortality
  • Neuroectodermal Tumors, Primitive, Peripheral / pathology*
  • Neurosecretory Systems / metabolism
  • Neurosecretory Systems / ultrastructure
  • RNA-Binding Protein EWS
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • S100 Proteins / metabolism
  • SOXE Transcription Factors / metabolism
  • Sarcoma, Clear Cell / pathology*
  • Survival Rate
  • Translocation, Genetic
  • United States / epidemiology
  • Vimentin / metabolism
  • Young Adult

Substances

  • ATF1 protein, human
  • Activating Transcription Factor 1
  • Biomarkers, Tumor
  • CREB1 protein, human
  • Calmodulin-Binding Proteins
  • Cyclic AMP Response Element-Binding Protein
  • EWSR1 protein, human
  • RNA-Binding Protein EWS
  • RNA-Binding Proteins
  • S100 Proteins
  • SOX10 protein, human
  • SOXE Transcription Factors
  • Vimentin