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      Clinicopathological and genomic analysis of double-hit follicular lymphoma: comparison with high-grade B-cell lymphoma with MYC and BCL2 and/or BCL6 rearrangements.

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          Abstract

          Most high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements are aggressive B-cell lymphomas. Occasional double-hit follicular lymphomas have been described but the clinicopathological features of these tumors are not well known. To clarify the characteristics of double-hit follicular lymphomas, we analyzed 10 cases of double-hit follicular lymphomas and 15 cases of high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements for clinicopathological and genome-wide copy-number alterations and copy-neutral loss-of-heterozygosity profiles. For double-hit follicular lymphomas, the median age was 67.5 years (range: 48-82 years). The female/male ratio was 2.3. Eight patients presented with advanced clinical stage. The median follow-up time was 20 months (range: 1-132 months). At the end of the follow-up, 8 patients were alive, 2 patients were dead including 1 patient with diffuse large B-cell lymphoma transformation. Rearrangements of MYC/BCL2, MYC/BCL6, and MYC/BCL2/BCL6 were seen in 8, 1, and 1 cases, respectively. The partner of MYC was IGH in 6 cases. There were no cases of histological grade 1, 4 cases of grade 2, 5 cases of grade 3a, and 1 case of grade 3b. Two cases of grade 3a exhibited immunoblast-like morphology. Immunohistochemistry demonstrated 9 cases with ≥50% MYC-positive cells. There was significant difference in MYC intensity (P=0.00004) and MIB-1 positivity (P=0.001) between double-hit follicular lymphomas and high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements. The genome profile of double-hit follicular lymphomas was comparable with conventional follicular lymphomas (GSE67385, n=198) with characteristic gains of 2p25.3-p11.1, 7p22.3-q36.3, 12q11-q24.33, and loss of 18q21.32-q23 (P<0.05). In comparison with high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements, double-hit follicular lymphomas had fewer copy-number alterations and minimal common region of gain at 2p16.1 (70%), locus also significant against conventional follicular lymphomas (P=0.0001). In summary, double-hit follicular lymphomas tended to be high-grade histology, high MYC protein expression, high MYC/IGH fusion, and minimal common region of gain at 2p16.1. Double-hit follicular lymphomas seemed to be a different disease from high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements and have an indolent clinical behavior similar to follicular lymphomas without MYC rearrangement.

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          Author and article information

          Journal
          Mod. Pathol.
          Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc
          Springer Science and Business Media LLC
          1530-0285
          0893-3952
          February 2018
          : 31
          : 2
          Affiliations
          [1 ] Department of Pathology, Tokai University School of Medicine, Isehara, Japan.
          [2 ] Department of Hematology/Oncology, Tokai University, School of Medicine, Isehara, Japan.
          [3 ] Department of Pathology, Kanagawa Cancer Center, Yokohama, Japan.
          [4 ] Department of Medical Oncology, Kanagawa Cancer Center, Yokohama, Japan.
          [5 ] Department of Pathology, St Marianna University School of Medicine, Kawasaki, Japan.
          [6 ] Division of Hematology and Oncology, St. Marianna University School of Medicine, Kawasaki, Japan.
          [7 ] Department of Pathology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama, Japan.
          [8 ] Department of Hematology, Endocrinology and Metabolism, Niigata University Faculty of Medicine, Niigata, Japan.
          [9 ] Department of Pathology and Hematopathology Unit, Hospital Clinic Barcelona, Molecular Pathology Laboratory, Institut d'Investigacions Biomediques August Pi i Sunyer (IDIBAPS), CIBER de Cancer (CIBERONIC), University of Barcelona, Barcelona, Spain.
          Article
          modpathol2017134
          10.1038/modpathol.2017.134
          28984304
          007e0647-c6ed-43d9-ba41-61d5589f0656

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