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Disease Discovery Classification of Lymphoid Neoplasms From www.bloodjournal.org by on December 4, 2008. For personal use only. 2008 112: 4384-4399 doi:10.1182/blood-2008-07-077982 Classification of lymphoid neoplasms: the microscope as a tool for disease discovery Elaine S. Jaffe, Nancy Lee Harris, Harald Stein and Peter G. Isaacson Updated information and services can be found at: http://bloodjournal.hematologylibrary.org/cgi/content/full/112/12/4384 Articles on similar topics may be found in the following Blood collections: Neoplasia (4200 articles) Free Research Articles (544 articles) ASH 50th Anniversary Reviews (32 articles) Clinical Trials and Observations (2473 articles) Information about reproducing this article in parts or in its entirety may be found online at: http://bloodjournal.hematologylibrary.org/misc/rights.dtl#repub_requests Information about ordering reprints may be found online at: http://bloodjournal.hematologylibrary.org/misc/rights.dtl#reprints Information about subscriptions and ASH membership may be found online at: http://bloodjournal.hematologylibrary.org/subscriptions/index.dtl Blood (print ISSN 0006-4971, online ISSN 1528-0020), is published semimonthly by the American Society of Hematology, 1900 M St, NW, Suite 200, Washington DC 20036. Copyright 2007 by The American Society of Hematology; all rights reserved. From www.bloodjournal.org by on December 4, 2008. For personal use only. ASH 50th anniversary review Classification of lymphoid neoplasms: the microscope as a tool for disease discovery Elaine S. Jaffe,1 Nancy Lee Harris,2 Harald Stein,3 and Peter G. Isaacson4 1Hematopathology Section, Laboratory of Pathology, Center for Cancer Research, National Cancer Institute, Bethesda, MD; 2Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston, MA; 3Institute for Pathology, Charite´ University Medicine, Campus Benjamin Franklin, Berlin, Germany; and 4Department of Histopathology, University College London Medical School, London, United Kingdom In the past 50 years, we have witnessed pathogenesis of lymphomas and lym- World Health Organization (WHO) classifi- explosive growth in the understanding of phoid leukemias are often based on the cation has been validated in international normal and neoplastic lymphoid cells. physiology of the lymphoid cells, capital- studies as being highly reproducible, and B-cell, T-cell, and natural killer (NK)–cell izing on deregulated normal physiology enhancing the interpretation of clinical neoplasms in many respects recapitulate by harnessing the promoters of genes and translational studies. In addition, ac- normal stages of lymphoid cell differentia- essential for lymphocyte function. The curate and precise classification of dis- tion and function, so that they can be to clinical manifestations of lymphomas like- ease entities facilitates the discovery of some extent classified according to the wise reflect the normal function of lym- the molecular basis of lymphoid neo- corresponding normal stage. Likewise, phoid cells in vivo. The multiparameter plasms in the basic science laboratory. the molecular mechanisms involved the approach to classification adopted by the (Blood. 2008;112:4384-4399) Introduction Mature B-cell and T/natural killer (NK)–cell neoplasms are clonal large cell lymphoma (ALCL),5 in which careful pathologic descrip- tumors of B cells, T cells, or NK cells that in many respects tions preceded the recognition of CCND1 and ALK, respectively, as recapitulate stages of normal B-cell or T-cell differentiation. genes critical to their pathogenesis. However, the process is Although classifications of lymphoid malignancies have histori- iterative, and once the underlying molecular cause is known, we cally treated lymphomas and leukemias separately, this distinction gain access to new diagnostic tools that help better define the is now appreciated as artificial. However, as the precursor neo- borderlines of the disease (Figure 1). Thus, the use of monoclonal plasms—lymphoblastic lymphomas/leukemias and acute myeloid antibodies reactive in routine sections to cyclin D1 and the ALK leukemias—are closely related from a clinical and biological tyrosine kinase helped define the morphologic spectrum of MCL perspective, they will not be covered in this review. In addition, and ALCL. This partnership between the pathologist and the plasma cell neoplasms often have been treated separately from molecular biologist is crucial in the classification of disease, and other lymphoid neoplasms, but this segregation is equally artificial, should be equally applicable to other organ systems. and the World Health Organization (WHO) classification of lymphoid neoplasms1 includes plasma disorders. A recent review by Kyle and Rajkumar in this series comprehensively Historical background: the early years discussed plasma cell myeloma,2 and thus we will not include it further in this review. The first description of what we now recognize as a lymphoma is As immunologists and pathologists have come to understand generally attributed to Thomas Hodgkin in 1832 (Table 2).46 The the ontogeny of lymphoid cells, it has been tempting to base the first use of the term lymphosarcoma is attributed to Rudolf Virchow classification of lymphoid malignancies strictly on the correspond- in 1863 (reviewed in Trumper et al8). In 1898 and 1902, Carl ing normal stage. However, some neoplasms—for example, hairy Sternberg and Dorothy Reed independently described the character- cell leukemia—do not clearly correspond to a normal B-cell istic binucleate and multinucleate giant cells that came to be called differentiation stage, and some clinically distinctive neoplasms the Reed-Sternberg or Sternberg-Reed cell.7 Sternberg felt that may exhibit immunophenotypic heterogeneity, such as hepato- Hodgkin disease was an inflammatory process, related to tuberculo- splenic T-cell lymphoma, which is derived from either ␣/␤ or ␥/␦ sis, but Reed disagreed.47 She made several other key observations: T cells. Thus, the normal counterpart of the neoplastic cell cannot at the general health of the patient before the onset of the disease is this time be the sole basis for classification. usually excellent; there was an early peak among children and Cancers are increasingly recognized as genetic diseases, with young adults; and Hodgkin disease usually presents as painless precise molecular alterations often defining entities. However, progressive cervical adenopathy without leukemia. She proposed progress in identifying the molecular pathogenesis of lymphoid that the pathologic picture is sufficient for diagnosis. Having malignancies has in most instances followed an accurate descrip- considerable success as a fellow in pathology, she sought a teaching tion of the disease by pathologists, based on morphologic, immuno- post at Johns Hopkins Medical School. Her chairman, William phenotypic and clinical parameters (Table 1). This paradigm is Welch, answered, “No women had ever held a teaching position in exemplified by both mantle cell lymphoma (MCL)3,4 and anaplastic the school, and there would be great opposition to it.”47 In her diary Submitted July 7, 2008; accepted August 20, 2008. DOI 10.1182/blood-2008- 07-077982. 4384 BLOOD, 1 DECEMBER 2008 ⅐ VOLUME 112, NUMBER 12 From www.bloodjournal.org by on December 4, 2008. For personal use only. BLOOD, 1 DECEMBER 2008 ⅐ VOLUME 112, NUMBER 12 CLASSIFICATION OF LYMPHOID NEOPLASMS 4385 Table 1. Pathogenetic insights based on a disease-oriented approach to lymphoma classification Lymphomas associated with infectious agents Nasal, cutaneous and systemic NK/T-cell lymphomas EBV Adult T-cell leukemia/lymphoma HTLV1 Marginal zone lymphomas H pylori, B burgdorferi, C jejuni, Hepatitis C, and others Primary effusion lymphoma, LBCL associated with multicentric CD HHV-8/ KSHV Plasmablastic, Burkitt, DLBCL, CHL EBV (subset of cases) Lymphomas with deregulation of apoptosis and survival pathways Follicular lymphoma BCL2/IGH@ MALT lymphomas API2/MALT1 and variants Lymphomas with deregulation of the cell cycle Mantle cell lymphoma CCND1/IGH@ Burkitt’s lymphoma MYC/IGH@ and variants Lymphomas with deregulation of cell signaling or transcriptional regulation Anaplastic large cell lymphoma NPM/ALK and variants Diffuse large B-cell lymphomas BCL6,NF␬B, Stat6 Lymphomas associated with host susceptibility factors, congenital or acquired Enteropathy-associated T-cell lymphoma Genetics, gliadin allergy Extranodal and systemic EBV ϩ T/NK cell lymphomas Genetics, host response to EBV Hepatosplenic T-cell lymphoma Immunosuppression combined with chronic antigenic stimulation Lymphomatoid granulomatosis Partial immune dysfunction and EBV Burkitt lymphoma Polyclonal B-cell activation with or without immunosuppression (malaria, HIV) Posttransplantation and other iatrogenic lymphoproliferative Iatrogenic immunosuppression disorders LBCL indicates large B-cell lymphoma. she noted, “Suddenly, as I saw what I had to face in acceptance of In 1925, Brill and colleagues described patients with enlarge- injustice—I knew that I couldn’t take it.”47 She left pathology and ment of lymph nodes and spleen, characterized pathologically by a took up a career in public health. proliferation of lymphoid follicles9; additional cases were reported The term “reticulum cell sarcoma” is attributed to Ewing, by Symmers,10 who also described progression to a large-cell Oberling, and Roulet, who each described tumors of large cells, neoplasm.11 In 1941, Edward A. Gall and Tracy B. Mallory, thought to be related to the supporting fibrous reticulum of pathologists
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