Annals of Oncology 10:1419-1432, 1999
© 1999 European Society for Medical Oncology
article-commentary |
The World Health Organization Classification of Neoplastic Diseases of the Hematopoietic and Lymphoid Tissues
Report of the Clinical Advisory Committee Meeting, Airlie House, Virginia, November, 1997
1Departments of Pathology. Massachusetts General Hospital and Harvard Medical School Boston, MA, USA
2National Cancer Institute Bethesda, MD, USA
3Hotel Dieu, Paris, France
4Hopital Necker Paris, France
5University of Wurzburg Wurzburg, Germany
6Pritzker School of Medicine, University of Chicago Chicago, IL, USA
7Department of Medical Oncology, St. Bartholomew's Hospital London, UK
8Ohio State University Comprehensive Cancer Center Columbus, OH, USA
Correspondence to: N. L. Harris, MD, Pathology, Warren 2, Massachusetts General Hospital, Fruit Street, Boston, MA 02114, USA E-mail: nlharris{at}partners.org
Introduction: Since 1995, the European Association of Pathologists (EAHP) and the Society for Hematopathology (SH) have been developing a new World Health Organization (WHO) Classification of hematologic malignancies. The classification includes lymphoid, myeloid, histiocytic, and mast cell neoplasms.
Design. The WHO project involves 10 committees of pathologists, who have developed lists and definitions of disease entities. A Clinical Advisory Committee (CAC) ) of international hematologists and oncologists was formed to ensure that the classification will be useful to clinicians. A meeting was held in November, 1997, to discuss clinical issues related to the classification.
Results: The WHO has adopted the ‘Revised European–American Classification of Lymphoid Neoplasms’ (R.E.A.L.), published in 1994 by the International Lymphoma Study Group (ILSG), as the classification of lymphoid neoplasms. This approach to classification is based on the principle that a classification is a list of ‘real’ disease entities, which are defined by a combination of morphology, immunophenotype, genetic features, and clinical features. The relative importance of each of these features varies among diseases, and there is no one ‘gold standard’. The WHO Classification has applied the principles of the R.E.A.L. Classification to myeloid and histiocytic neoplasms. The classification of myeloid neoplasms recognizes distinct entities defined by a combination of morphology and cytogenetic abnormalities.
The CAC meeting, which was organized around a series of clinical questions, was able to reach a consensus on most of the questions posed. The questions and the consensus are discussed in detail below. Among other things, the CAC concluded that clinical groupings of lymphoid neoplasms were neither necessary nor desirable. Patient treatment is determined by the specific type of lymphoma, with the addition of grade within the tumor type, if applicable, and clinical prognostic factors such as the international prognostic index (IPI).
Conclusion: The experience of developing the WHO Classification has produced a new and exciting degree of cooperation and communication between oncologists and pathologists from around the world, which should facilitate progress in the understanding and treatment of hematologic malignancies.
classification, histiocytic, lymphoma, leukemia, myeloid, mast cell
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  T. Barbui, A. Carobbio, F. Cervantes, A. M. Vannucchi, P. Guglielmelli, E. Antonioli, A. Alvarez-Larran, A. Rambaldi, G. Finazzi, and G. Barosi Thrombosis in primary myelofibrosis: incidence and risk factors Blood, January 28, 2010; 115(4): 778 - 782. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Kantarjian, P. Fenaux, M. A. Sekeres, P. S. Becker, A. Boruchov, D. Bowen, E. Hellstrom-Lindberg, R. A. Larson, R. M. Lyons, P. Muus, et al. Safety and Efficacy of Romiplostim in Patients With Lower-Risk Myelodysplastic Syndrome and Thrombocytopenia J. Clin. Oncol., January 20, 2010; 28(3): 437 - 444. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. E. Balatoni, D. W. Dawson, J. Suh, M. H. Sherman, G. Sanders, J. S. Hong, M. J. Frank, C. S. Malone, J. W. Said, and M. A. Teitell Epigenetic Silencing of Stk39 in B-Cell Lymphoma Inhibits Apoptosis from Genotoxic Stress Am. J. Pathol., October 1, 2009; 175(4): 1653 - 1661. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Psyrri, S. Papageorgiou, E. Liakata, A. Scorilas, D. Rontogianni, C. K. Kontos, P. Argyriou, D. Pectasides, N. Harhalakis, V. Pappa, et al. Phosphatidylinositol 3'-Kinase Catalytic Subunit {alpha} Gene Amplification Contributes to the Pathogenesis of Mantle Cell Lymphoma Clin. Cancer Res., September 15, 2009; 15(18): 5724 - 5732. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Tholouli, S. Watt, G. S. Lucas, J. Burthem, J. A. L. Yin, J. Cavet, H. Greenfield, and J. B. Houghton Stage IV adult sporadic Burkitt lymphoma/leukemia with complex bone marrow cytogenetics is associated with a very poor outcome Blood, July 9, 2009; 114(2): 485 - 486. [Full Text] [PDF]
|
|
|
|
|
|
S. Quijano, A. Lopez, J. Manuel Sancho, C. Panizo, G. Deben, C. Castilla, J. Antonio Garcia-Vela, A. Salar, N. Alonso-Vence, E. Gonzalez-Barca, et al. Identification of Leptomeningeal Disease in Aggressive B-Cell Non-Hodgkin's Lymphoma: Improved Sensitivity of Flow Cytometry J. Clin. Oncol., March 20, 2009; 27(9): 1462 - 1469. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. A. Wang, O. Pozdnyakova, J. L. Jorgensen, L. J. Medeiros, D. Stachurski, M. Anderson, A. Raza, and B. A. Woda Detection of paroxysmal nocturnal hemoglobinuria clones in patients with myelodysplastic syndromes and related bone marrow diseases, with emphasis on diagnostic pitfalls and caveats Haematologica, January 1, 2009; 94(1): 29 - 37. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Sekeres, J. P. Maciejewski, A. A.N. Giagounidis, K. Wride, R. Knight, A. Raza, and A. F. List Relationship of Treatment-Related Cytopenias and Response to Lenalidomide in Patients With Lower-Risk Myelodysplastic Syndromes J. Clin. Oncol., December 20, 2008; 26(36): 5943 - 5949. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. S. LaCasce, M. E. Kho, J. W. Friedberg, J. C. Niland, G. A. Abel, M. A. Rodriguez, M. S. Czuczman, M. M. Millenson, A. D. Zelenetz, and J. C. Weeks Comparison of Referring and Final Pathology for Patients With Non-Hodgkin's Lymphoma in the National Comprehensive Cancer Network J. Clin. Oncol., November 1, 2008; 26(31): 5107 - 5112. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A V Martin and B Sharma Positron emission tomography and CT in the management of lymphoma Imaging, September 1, 2008; 20(3): 169 - 175. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-J. Goval, C. Thielen, C. Bourguignon, R. Greimers, E. Dejardin, Y. S. Choi, J. Boniver, and L. de Leval The prevention of spontaneous apoptosis of follicular lymphoma B cells by a follicular dendritic cell line: involvement of caspase-3, caspase-8 and c-FLIP Haematologica, August 1, 2008; 93(8): 1169 - 1177. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Quijano, A. Lopez, A. Rasillo, S. Barrena, M. Luz Sanchez, J. Flores, C. Fernandez, J. M. Sayagues, C. S. Osuna, N. Fernandez, et al. Association between the proliferative rate of neoplastic B cells, their maturation stage, and underlying cytogenetic abnormalities in B-cell chronic lymphoproliferative disorders: analysis of a series of 432 patients Blood, May 15, 2008; 111(10): 5130 - 5141. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Yamanaka, K. Morii, Y. Shinbo, J. Homma, M. Sano, N. Tsuchiya, N. Yajima, T. Tamura, H. Hondoh, H. Takahashi, et al. Results of Treatment of 112 Cases of Primary CNS Lymphoma Jpn. J. Clin. Oncol., May 1, 2008; 38(5): 373 - 380. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G Kapatai and P Murray Contribution of the Epstein Barr virus to the molecular pathogenesis of Hodgkin lymphoma J. Clin. Pathol., December 1, 2007; 60(12): 1342 - 1349. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Dicker, C. Haferlach, W. Kern, T. Haferlach, and S. Schnittger Trisomy 13 is strongly associated with AML1/RUNX1 mutations and increased FLT3 expression in acute myeloid leukemia Blood, August 15, 2007; 110(4): 1308 - 1316. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-L. Harousseau, J. E. Lancet, J. Reiffers, B. Lowenberg, X. Thomas, F. Huguet, P. Fenaux, S. Zhang, W. Rackoff, P. De Porre, et al. A phase 2 study of the oral farnesyltransferase inhibitor tipifarnib in patients with refractory or relapsed acute myeloid leukemia Blood, June 15, 2007; 109(12): 5151 - 5156. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Creutzig, M. Zimmermann, T. Lehrnbecher, N. Graf, J. Hermann, C. M. Niemeyer, A. Reiter, J. Ritter, M. Dworzak, J. Stary, et al. Less Toxicity by Optimizing Chemotherapy, but Not by Addition of Granulocyte Colony-Stimulating Factor in Children and Adolescents With Acute Myeloid Leukemia: Results of AML-BFM 98 J. Clin. Oncol., September 20, 2006; 24(27): 4499 - 4506. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Pellagatti, M. Cazzola, A. A. N. Giagounidis, L. Malcovati, M. G. D. Porta, S. Killick, L. J. Campbell, L. Wang, C. F. Langford, C. Fidler, et al. Gene expression profiles of CD34+ cells in myelodysplastic syndromes: involvement of interferon-stimulated genes and correlation to FAB subtype and karyotype Blood, July 1, 2006; 108(1): 337 - 345. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Pagano, A. Gallamini, G. Trape, L. Fianchi, D. Mattei, G. Todeschini, A. Spadea, S. Cinieri, E. Iannitto, M. Martelli, et al. NK/T-cell lymphomas 'nasal type': an Italian multicentric retrospective survey Ann. Onc., May 1, 2006; 17(5): 794 - 800. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. P. Treon, Z. R. Hunter, A. Aggarwal, E. P. Ewen, S. Masota, C. Lee, D. D. Santos, E. Hatjiharissi, L. Xu, X. Leleu, et al. Characterization of familial Waldenstrom's macroglobulinemia Ann. Onc., March 1, 2006; 17(3): 488 - 494. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Sokol and T. P. Loughran Jr. Large granular lymphocyte leukemia. Oncologist, March 1, 2006; 11(3): 263 - 273. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Rizvi, A. M. Evens, M. S. Tallman, B. P. Nelson, and S. T. Rosen T-cell non-Hodgkin lymphoma Blood, February 15, 2006; 107(4): 1255 - 1264. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H.-J. Chiou, Y.-H. Chou, S.-Y. Chiou, W.-M. Chen, W. Chen, H.-K. Wang, and C.-Y. Chang High-Resolution Ultrasonography of Primary Peripheral Soft Tissue Lymphoma J. Ultrasound Med., January 1, 2005; 24(1): 77 - 86. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Kuendgen, C. Strupp, M. Aivado, A. Bernhardt, B. Hildebrandt, R. Haas, U. Germing, and N. Gattermann Treatment of myelodysplastic syndromes with valproic acid alone or in combination with all-trans retinoic acid Blood, September 1, 2004; 104(5): 1266 - 1269. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. T. Hehn, T. M. Grogan, and T. P. Miller Utility of Fine-Needle Aspiration As a Diagnostic Technique in Lymphoma J. Clin. Oncol., August 1, 2004; 22(15): 3046 - 3052. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kewalramani, A. D. Zelenetz, S. D. Nimer, C. Portlock, D. Straus, A. Noy, O. O'Connor, D. A. Filippa, J. Teruya-Feldstein, A. Gencarelli, et al. Rituximab and ICE as second-line therapy before autologous stem cell transplantation for relapsed or primary refractory diffuse large B-cell lymphoma Blood, May 15, 2004; 103(10): 3684 - 3688. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. D. Jones, K. H. Darnell, R. A. Warnke, and J. L. Zehnder CyclinD1/CyclinD3 Ratio by Real-Time PCR Improves Specificity for the Diagnosis of Mantle Cell Lymphoma J. Mol. Diagn., May 1, 2004; 6(2): 84 - 89. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. A. Leitch, R. D. Gascoyne, M. Chhanabhai, N. J. Voss, R. Klasa, and J. M. Connors Limited-stage mantle-cell lymphoma Ann. Onc., October 1, 2003; 14(10): 1555 - 1561. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. S. Reading, S. D. Jenson, J. K. Smith, M. S. Lim, and K. S. J. Elenitoba-Johnson 5'-(RACE) Identification of Rare ALK Fusion Partner in Anaplastic Large Cell Lymphoma J. Mol. Diagn., May 1, 2003; 5(2): 136 - 140. [Full Text] [PDF]
|
|
|
|
|
|
S Nakamura, T Matsumoto, S Nakamura, Y Jo, K Fujisawa, H Suekane, T Yao, M Tsuneyoshi, and M Iida Chromosomal translocation t(11;18)(q21;q21) in gastrointestinal mucosa associated lymphoid tissue lymphoma J. Clin. Pathol., January 1, 2003; 56(1): 36 - 42. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. M. Maggio, A. van den Berg, D. de Jong, A. Diepstra, and S. Poppema Low Frequency of FAS Mutations in Reed-Sternberg Cells of Hodgkin's Lymphoma Am. J. Pathol., January 1, 2003; 162(1): 29 - 35. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Mufti, A. F. List, S. D. Gore, and A. Y.L. Ho Myelodysplastic Syndrome Hematology, January 1, 2003; 2003(1): 176 - 199. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. J. Lee, J.-G. Im, J. M. Goo, K. W. Kim, B. I. Choi, K. H. Chang, J. K. Han, and M. H. Han Peripheral T-Cell Lymphoma: Spectrum of Imaging Findings with Clinical and Pathologic Features RadioGraphics, January 1, 2003; 23(1): 7 - 26. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. M. Tsimberidou, P. McLaughlin, A. Younes, M. A. Rodriguez, F. B. Hagemeister, A. Sarris, J. Romaguera, M. Hess, T. L. Smith, Y. Yang, et al. Fludarabine, mitoxantrone, dexamethasone (FND) compared with an alternating triple therapy (ATT) regimen in patients with stage IV indolent lymphoma Blood, December 15, 2002; 100(13): 4351 - 4357. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P L Roddam, S Rollinson, M O'Driscoll, P A Jeggo, A Jack, and G J Morgan Genetic variants of NHEJ DNA ligase IV can affect the risk of developing multiple myeloma, a tumour characterised by aberrant class switch recombination J. Med. Genet., December 1, 2002; 39(12): 900 - 905. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. M. Mead, M. R. Sydes, J. Walewski, A. Grigg, C. S. Hatton, P. Norbert, C. Guarnaccia, M. S. Lewis, J. McKendrick, S. P. Stenning, et al. An international evaluation of CODOX-M and CODOX-M alternating with IVAC in adult Burkitt's lymphoma: results of United Kingdom Lymphoma Group LY06 study Ann. Onc., August 1, 2002; 13(8): 1264 - 1274. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Albitar, T. Manshouri, Y. Shen, D. Liu, M. Beran, H. M. Kantarjian, A. Rogers, I. Jilani, C. W. Lin, S. Pierce, et al. Myelodysplastic syndrome is not merely "preleukemia" Blood, July 18, 2002; 100(3): 791 - 798. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Montoto, A. Lopez-Guillermo, A. Ferrer, M. Camos, A. Alvarez-Larran, F. Bosch, J. Blade, F. Cervantes, J. Esteve, F. Cobo, et al. Survival after progression in patients with follicular lymphoma: analysis of prognostic factors Ann. Onc., April 1, 2002; 13(4): 523 - 530. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Bertoni, A. Conconi, C. Capella, T. Motta, R. Giardini, M. Ponzoni, E. Pedrinis, D. Novero, P. Rinaldi, G. Cazzaniga, et al. Molecular follow-up in gastric mucosa-associated lymphoid tissue lymphomas: early analysis of the LY03 cooperative trial Blood, April 1, 2002; 99(7): 2541 - 2544. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Nanjangud, P. H. Rao, A. Hegde, J. Teruya-Feldstein, G. Donnelly, J. Qin, S. C. Jhanwar, A. D. Zelenetz, and R. S. K. Chaganti Spectral karyotyping identifies new rearrangements, translocations, and clinical associations in diffuse large B-cell lymphoma Blood, April 1, 2002; 99(7): 2554 - 2561. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Z. Rassidakis, L. J. Medeiros, T. J. McDonnell, S. Viviani, V. Bonfante, G. Nadali, T. P. Vassilakopoulos, R. Giardini, M. Chilosi, C. Kittas, et al. BAX Expression in Hodgkin and Reed-Sternberg Cells of Hodgkin's Disease: Correlation with Clinical Outcome Clin. Cancer Res., February 1, 2002; 8(2): 488 - 493. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. N. Shenkier, N. Voss, R. Fairey, R. D. Gascoyne, P. Hoskins, R. Klasa, P. Klimo, S. E. O'Reilly, S. Sutcliffe, and J. M. Connors Brief Chemotherapy and Involved-Region Irradiation for Limited-Stage Diffuse Large-Cell Lymphoma: An 18-Year Experience From the British Columbia Cancer Agency J. Clin. Oncol., January 1, 2002; 20(1): 197 - 204. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Martinez-Climent, E. Vizcarra, D. Sanchez, D. Blesa, I. Marugan, I. Benet, F. Sole, F. Rubio-Moscardo, M. J. Terol, J. Climent, et al. Loss of a novel tumor suppressor gene locus at chromosome 8p is associated with leukemic mantle cell lymphoma Blood, December 1, 2001; 98(12): 3479 - 3482. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Bellosillo, N. Villamor, A. Lopez-Guillermo, S. Marce, J. Esteve, E. Campo, D. Colomer, and E. Montserrat Complement-mediated cell death induced by rituximab in B-cell lymphoproliferative disorders is mediated in vitro by a caspase-independent mechanism involving the generation of reactive oxygen species Blood, November 1, 2001; 98(9): 2771 - 2777. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. K. Magnusson, K. E. Meade, K. E. Brown, D. C. Arthur, L. A. Krueger, A. J. Barrett, and C. E. Dunbar Rabaptin-5 is a novel fusion partner to platelet-derived growth factor {beta} receptor in chronic myelomonocytic leukemia Blood, October 15, 2001; 98(8): 2518 - 2525. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C Montalban, A Santon, D Boixeda, and C Bellas Regression of gastric high grade mucosa associated lymphoid tissue (MALT) lymphoma after Helicobacter pylori eradication Gut, October 1, 2001; 49(4): 584 - 587. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Z. Rassidakis, A. H. Sarris, M. Herling, R. J. Ford, F. Cabanillas, T. J. McDonnell, and L. J. Medeiros Differential Expression of BCL-2 Family Proteins in ALK-Positive and ALK-Negative Anaplastic Large Cell Lymphoma of T/Null-Cell Lineage Am. J. Pathol., August 1, 2001; 159(2): 527 - 535. [Abstract] [Full Text]
|
|
|
|
|
|
A. Conconi, F. Bertoni, E. Pedrinis, T. Motta, E. Roggero, S. Luminari, C. Capella, M. Bonato, F. Cavalli, and E. Zucca Nodal marginal zone B-cell lymphomas may arise from different subsets of marginal zone B lymphocytes Blood, August 1, 2001; 98(3): 781 - 786. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Willenbrock, A. Roers, C. Seidl, H.-H. Wacker, R. Kuppers, and M.-L. Hansmann Analysis of T-Cell Subpopulations in T-Cell Non-Hodgkin's Lymphoma of Angioimmunoblastic Lymphadenopathy with Dysproteinemia Type by Single Target Gene Amplification of T Cell Receptor- {beta} Gene Rearrangements Am. J. Pathol., May 1, 2001; 158(5): 1851 - 1857. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Connors, E. M. Noordijk, and S. J. Horning Hodgkin's Lymphoma: Basing the Treatment on the Evidence Hematology, January 1, 2001; 2001(1): 178 - 193. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Cavalli, P. G. Isaacson, R. D. Gascoyne, and E. Zucca MALT Lymphomas Hematology, January 1, 2001; 2001(1): 241 - 258. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Zucca, F. Bertoni, E. Roggero, and F. Cavalli The gastric marginal zone B-cell lymphoma of MALT type Blood, July 15, 2000; 96(2): 410 - 419. [Full Text] [PDF]
|
|