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An Overview of the Classification of Non-Hodgkin's Lymphomas: an Integration of Morphological and Phenotypical Concepts1

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An Overview of the Classification of Non-Hodgkin's Lymphomas: an Integration of Morphological and Phenotypical Concepts1 [CANCER RESEARCH (SUPPL.) 52, 5447s-5452s. October I. 1992| An Overview of the Classification of Non-Hodgkin's Lymphomas: An Integration of Morphological and Phenotypical Concepts1 Elaine S. Jaffe,2 Mark Raffeid, L. Jeffrey Medeiros, and Maryalice Stetler-Stevenson Hematopathology Section, Laboratory of Pathology, National Cancer Institute, NIH, Bethesda, Maryland 20982 Abstract As a result of this dissatisfaction, a variety of classification An analysis of trends in the incidence of non-Hodgkin's lymphoma schemes were proposed. Two of them, the Lukes and Collins Classification (3) and the Kiel Scheme (4), as proposed by Len- requires an understanding of individual disease entities within this broad group. The non-Hodgkin's lymphomas represent a diverse group nert and colleagues, are shown in Table 1. The complexity of of malignancies that have in common an origin from lymphoid cells. this terminology is obvious. All of these terms have been in Nevertheless, these disorders are heterogeneous in their clinical behav International Classification of Diseases for Oncology, and ior, morphological appearance, cellular origin, etiology, and pathogen- probably all are reflected in the SEER data at one point or esis. A modern classification of non-Hodgkin's lymphomas must include another. Moreover, if one tries to discern individual disease an integration of morphological, immunophenotypical, and molecular entities from these data, it is virtually impossible. concepts in order to delineate individual diseases within this broad The National Cancer Institute responded to this problem by group. Existing classification schemes such as the working formulation, funding a study to test the six major classification schemes while they may be useful in providing a guide to clinical management, cannot provide this information in the absence of other data. proposed at this time. They examined 1175 cases of lymphoma This point is most readily made with the low-grade B-cell lymphomas that had been prospectively staged and treated in a uniform which include follicular lymphomas, mantle cell lymphomas, small lym- manner at one of four major treatment centers (5). Not surpris phocytic lymphomas, immunosecretory disorders, and lymphomas of ingly, all six classification schemes could identify tumors of mucosa-associated lymphoid tissues. Each of these malignancies has a low- or high-grade clinical behavior, and no one scheme seemed distinct phenotype and genotype, and indubitably each has a different to work significantly better than any other. etiology. The postthymic T-cell tumors are equally diverse. Analysis of Consequently, the investigators involved in that study pro epidemiológica! data from cancer registries must include a recognition posed a working formulation for non-Hodgkin's lymphoma di that our ability to recognize individual diseases from historical data is limited. Studies of trends in the non-Hodgkin's lymphomas should at agnosis, and they divided the tumors into morphological groups tempt to delineate biological markers that may be of relevance to patho- ranked according to their clinical behavior in these 1175 cases genesis in both historical and prospectively accrued cases. (Table 2). At the time that the working formulation was pub lished, the authors (5) of it stated that it was "not proposed as a new classification, but as a means of translation among the Introduction various systems." Unfortunately, this subtle distinction has not The non-Hodgkin's lymphomas are not a single disease always been appreciated. but represent a diverse group of clinicopathological and biolog The working formulation categories do not identify individ ical entities. The modern approach to lymphoma diagnosis ual disease entities. The terms that it uses are microscopic should include both morphological and phenotypic techniques. descriptors. They describe the cellular population that the pa The Rappaport classification is not in current use; however, thologist sees in the histológica! section, but one cannot infer when this classification scheme was proposed in the 1960s, it that each category is an individual disease. In fact, we have very immediately became popular among clinicians and is the ter good evidence today that most of these categories do not rep minology that has been most widely utilized in the Surveillance resent individual diseases. If one wishes to understand the ep Epidemiology and End Results program (SEER) data base (Ta idemiology of lymphomas and to understand time trends, one ble 1)(1). The classification of non-Hodgkin's lymphomas, as proposed must step away from this approach and look at individual dis by Rappaport (1), first divided lymphomas according to their eases rather than morphological categories. architectural pattern, nodular or diffuse, and then according to Essential to this process is the use of immunological ap the cytological cell type. If the cells were small, they were proaches. The malignant lymphomas are tumors of the immune termed "lymphocytic," or if large, "histiocytic." However, dur system, and the malignant cells retain both the phenotypic and ing the 1970s when the field of immunology was undergoing a functional properties of their precursors. Using the tools of rapid expansion, the scientific basis for this scheme came into immunology, we can begin to dissect out individual diseases question. It became apparent that the large cell tumors that among the malignant lymphomas. Rappaport termed histiocytic were, in fact, composed of trans The development of monoclonal antibodies has been invalu formed lymphoid cells. Furthermore, the Rappaport scheme able in providing us with a battery of reagents that can be did not take into consideration the phenotypic heterogeneity of consistently used among different laboratories. Most of these the immune system as it related to the classification of lympho reagents have to be applied to freshly isolated cells, either in cell mas (2). suspension or in frozen sections, but increasingly, monoclonal antibodies are available that can be used on routinely processed paraffin-embedded sections (6). These reagents provide an im 1 Presented at the National Cancer Institute Workshop, "The Emerging Epi portant step in permitting the use of these techniques on a demic of Non-Hodgkin's Lymphoma: Current Knowledge Regarding Etiological routine basis for most lymphomas. Factors," October 22-23, 1991, Bethesda. MD. The vast majority of non-Hodgkin's lymphomas diagnosed in 2 To whom requests for reprints should be addressed, at Hematopathology Sec tion, Laboratory of Pathology, National Cancer Institute, Bethesda, MD 20982. the United States and in Europe are of B-cell origin and fall into 5447s Downloaded from cancerres.aacrjournals.org on September 23, 2021. © 1992 American Association for Cancer Research. CLASSIFICATION OF NON-HODGKIN'S LYMPHOMAS Table 1 Comparison of commonly used classifications for non-Hodgkin's lymphomas Modified Rappaport Working Lukes and Collins Working Working classification formulation" classification formulation Kiel classification formulation Nodular Undefined cell type Low-grade malignancy Lymphocytic, well differentiated A T-cell type, small lymphocytic A Lymphocytic, chronic lymphocytic/ Lymphocytic, poorly B T-cell type, Sézary-mycosisfungoides leukemia A differentiated C (cerebriform) Lymphocytic, other A Mixed, lymphocytic and histiocytic D T-cell type, convoluted lymphocytic I Lymphoplasmacytoid A Histiocytic T-cell type, immunoblastic sarcoma Centrocytic E Diffuse (T-cell) H Centroblastic-centrocytic, follicular Lymphocytic, well differentiated A B-cell type, small lymphocytic A without sclerosis B, C without plasmacytoid features B-cell type, plasmacytoid lymphocytic A Centroblastic-centrocytic, follicular D Lymphocytic, well differentiated A Follicular center cell, small cleaved B-E with sclerosis with plasmacytoid features E Follicular center cell, large cleaved D-G Centroblastic-centrocytic, follicular Lymphocytic, poorly I Follicular center cell, small J and diffuse, without sclerosis differentiated I noncleaved D-G Centroblastic-centrocytic, follicular Lymphoblastic, convoluted F Follicular center cell, large and diffuse, with sclerosis Lymphoblastic, nonconvoluted G noncleaved Centroblastic-centrocytic, diffuse Mixed, lymphocytic and histioytic G Immunoblastic sarcoma (B-cell) H Low-grade malignant lymphoma, F Histiocytic without sclerosis J Subtypes of follicular center cell unclassified Histiocytic with sclerosis J lymphomas High-grade malignancy Burkitt's tumor 1. Follicular Centroblastic Undifferentiated 2. Follicular and diffuse Lymphoblastic, Burkitt's type G Malignant lymphoma, unclassified 3. Diffuse Lymphoblastic, convoluted cell type J Composite lymphoma 4. Sclerotic with follicles Lymphoblastic, other (classified) I 5. Sclerotic without follicles Immunoblastic Histiocytic High-grade malignant lymphoma, H Malignant lymphoma, unclassified unclassified Malignant lymphoma, unclassified (unable to specify "high grade" or "low grade") Composite lymphoma " Letters indicate equivalent or related category in the working formulation as shown in Table 2. Table 2 National Cancer Institute working formulation of non-Hodgkin's Follicular lymphoma is the prototype of the low-grade B-cell lymphomas for clinical usage (Ref. 5) lymphomas and is the single largest group of non-Hodgkin's Low grade A. Small lymphocytic lymphomas, accounting for approximately 45% of all cases (5). B. Follicular, predominantly small cleaved cell It is a disease
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