Abstract
A clinicopathological study of 515 non‐Hodgkin's lymphoma (NHL) cases was performed using the revised European‐American classification of lymphoid neoplasms (REAL classification) in an HTLV1‐nonendemic area of Japan. The following characteristics were revealed: 1) frequency of extranodal lymphomas was high (59%) with 79% B‐cell lymphomas in this series, while the overall ratio of B:T/NK lineage was 3.7:1; 2) the most common type was the diffuse large B‐cell lymphoma (46%), follicle center lymphomas occurred at an incidence lower (15%) than that in European and American populations, and marginal zone B‐cell lymphomas accounted for as much as 12%; 3) peripheral T‐cell lymphomas were common (19%), with the unspecified type predominant (11%), while adult T‐cell lymphomas were present at a level equivalent to that among European and American patients (1%). Clear segregation of survival curves was rated according to cell lineage and B‐cell lymphomas had a better prognosis than T/NK‐cell lymphomas. Furthermore, new subtypes in the REAL classification, such as marginal zone B‐cell and mantle cell lymphomas, exhibited distinct curves. Taken altogether, the REAL classification demonstrated advantages for assessment of Japanese NHL cases.
Keywords: Lymphoma, REAL classification, Non‐Hodgkin's lymphoma
Full Text
The Full Text of this article is available as a PDF (101.9 KB).
REFERENCES
- 1. ) Harris , N. L. , Jaffe , E. S. , Stein , H. , Banks , P. M. , Chan , J. K. C. , Cleary , M. L. , Delsol , G. , Wolf‐Peeters , C. D. , Falini , B. , Gatter , K. C. , Grogan , T. M. , Isaacson , P. G. , Knowles , D. M. , Mason , D. Y. , Muller‐Hermelink , H. S. , Pileri , S. A. , Piris , M. A. , Ralfkiaer , E. and Warnke , R. A.A revised European‐American classification of lymphoid neoplasms: a proposal from the international lymphoma study group . Blood , 84 , 1361 – 1392 ( 1994. ). [PubMed] [Google Scholar]
- 2. ) Lennert , K. and Feller , A. C.“Histopathology of Non‐Hodgkin's Lymphomas (Based on the Updated Kiel Classification) ,” 2nd Ed. ( 1992. ). Springer‐Verlag; , New York, Berlin and Heidelberg . [Google Scholar]
- 3. ) Fisher , R. I. , Grogan , T. M. , Dahlberg , S. , Braziel , R. , Banks , P. , Nathwani , B. , Kjeldsberg , C. and Miller , T. P.Clinical behavior of 2,168 patients treated on Southwest Oncology Group (SWOG) protocols and reclassified according to the R.E.A.L. classification . Ann. Oncol. , 7 ( Suppl. 3 ), 3 ( 1996. ). [Google Scholar]
- 4. ) Pittaluga , S. , Bijnens , L. , Teodorovic , I. , Hagenbeek , A. , Meerwaldt , J. H. , Somers , R. , Thomas , J. , Noordijk , E. M. and Wolf‐Peeters , C. D.Clinical analysis of 670 cases in two trials of the European Organization for the Research and Treatment of Cancer Lymphoma Cooperative Group subtyped according to the revised European‐American Classification of Lymphoid Neoplasms: a Comparison with the Working Formulation . Blood , 87 , 4358 – 4367 ( 1996. ). [PubMed] [Google Scholar]
- 5. ) The Non‐Hodgkin's Lymphoma Classification Project . A clinical evaluation of the International Lymphoma Study Group classification of non‐Hodgkin's lymphoma . Blood , 89 , 3909 – 3918 ( 1997. ). [PubMed] [Google Scholar]
- 6. ) Melnyk , A. , Rodriguez , A. , Pugh , W. C. and Cabannillas , F.Evaluation of the Revised European‐American Lymphoma Classification confirms the clinical relevance of immunophenotype in 560 cases of aggressive non‐Hodgkin's lymphoma . Blood , 89 , 4514 – 4520 ( 1997. ). [PubMed] [Google Scholar]
- 7. ) Salar , A. , Fernandez de Sevilla , A. , Romagosa , V. , Domingo‐Claros , A. , Gonzalez‐Barca , E. , De Sanjose , S. , Pera , J. , Servitje , O. and Granena , A.Distribution and incidence rates of lymphoid neoplasms according to the REAL classification in a single institution. A prospective study of 940 cases . Eur. J. Haematol. , 59 , 231 – 237 ( 1997. ). [DOI] [PubMed] [Google Scholar]
- 8. ) Suchi , T. , Tajima , K. , Nanba , K. , Wakasa , H. , Mikata , A. , Kikuchi , M. , Mori , S. , Watanabe , S. , Mohri , N. , Shamoto , M. , Harigaya , K. , Itagaki , T. , Matsuda , M. , Kirino , Y. , Takagi , K. and Fukunaga , S.Some problems on the histopathological diagnosis of non‐Hodgkin's malignant lymphoma—a proposal of a new type— . Acta Pathol. Jpn. , 29 , 755 – 776 ( 1979. ). [DOI] [PubMed] [Google Scholar]
- 9. ) Banks , P. M. , Chan , J. , Cleary , M. L. , Delsol , G. , De Wolf‐Peeters , C. , Gatter , K. , Grogan , T. M. , Harris , N. L. , Isaacson , P. G. , Jaffe , E. S. , Mason , D. , Pileri , S. , Ralfkiaer , E. , Stein , H. and Warnke , R. A.Mantle cell lymphoma: a proposal for unification of morphologic, immunologic, and molecular data . Am. J. Surg. Pathol. , 16 , 637 – 640 ( 1992. ). [DOI] [PubMed] [Google Scholar]
- 10. ) Issacson , P. and Wright , D. H.Extranodal malignant lymphoma arising from mucosa‐associated lymphoid tissue . Cancer , 53 , 2515 – 2514 ( 1984. ). [DOI] [PubMed] [Google Scholar]
- 11. ) Issacson , P. G. and Spencer , J.Malignant lymphoma of mucosa‐associated lymphoid tissue . Histopathology , 11 , 445 – 462 ( 1987. ). [DOI] [PubMed] [Google Scholar]
- 12. ) Carbone , P. P. , Kaplan , H. S. , Musshof , K. , Smithers , D. W. and Tubiana , M.Report of the committee on Hodgkin's disease staging classification . Cancer Res. , 31 , 1860 – 1861 ( 1971. ). [PubMed] [Google Scholar]
- 13. ) Isaacson , P. G. and Norton , A. J.“Extranodular Lymphomas ,” pp. 1 – 4 ( 1994. ). Churchill Livingstone; , Edinburgh . [Google Scholar]
- 14. ) West , K. P. , Warford , A. , Fray , L. and Allen , M.The demonstration of B‐cell, T‐cell and myeloid antigens in paraffin sections . J. Pathol. , 150 , 89 – 101 ( 1986. ). [DOI] [PubMed] [Google Scholar]
- 15. ) Braylan , R. C. and Benson , N. A.Flow cytometric analysis of lymphomas . Arch. Pathol. Lab. Med. , 113 , 627 – 633 ( 1989. ). [PubMed] [Google Scholar]
- 16. ) Maseki , N. , Kaneko , Y. , Sakurai , M. , Kurihara , M. , Sampi , K. , Shimamura , K. and Takayama , S.Chromosome abnormalities in malignant lymphoma in patients from Saitama . Cancer Res. , 47 , 6767 – 6775 ( 1987. ). [PubMed] [Google Scholar]
- 17. ) Southern , E. M.Detection of specific sequences among DNA fragments separated by gel electrophoresis . J. Mol. Biol. , 98 , 503 – 517 ( 1975. ). [DOI] [PubMed] [Google Scholar]
- 18. ) Hiddemann , W. , Longo , D. L. , Coiffier , B. , Fisher , R. I. , Cabanillas , F. , Cavalli , F. , Nadler , L. M. , De Vita , V. T. , Lister , T. A. and Armitage , J. O.Lymphoma classification—The gap between biology and clinical management is closing . Blood , 88 , 4085 – 4089 ( 1996. ). [PubMed] [Google Scholar]
- 19. ) Frizzera , G.Recent progress in lymphoma classification . Curr. Opin. Oncol. , 9 , 392 – 402 ( 1997. ). [DOI] [PubMed] [Google Scholar]
- 20. ) Harris , N. L.Principles of the revised European‐American Lymphoma Classification (from the International Lymphoma Study Group) . Ann. Oncol. , 8 , 11 – 16 ( 1997. ). [PubMed] [Google Scholar]
- 21. ) Aozasa , K. , Tsujimoto , M. , Sakurai , M. , Honda , M. , Yamashita , K. , Hanada , M. and Sugimoto , A.Non‐Hodgkin's lymphomas in Osaka, Japan . Eur. J. Cancer Clin. Oncol. , 21 , 487 – 492 ( 1985. ). [DOI] [PubMed] [Google Scholar]
- 22. ) Mohri , N.Extranodal lymphoma . In“Current Encyclopedia of Pathology 18b ,” ed. Iijima S. , Ishikawa H. , Kageyama K. , Shimamine T. and Mori W. , pp. 119 – 138 ( 1987. ). Nakayama‐Shoten; , Tokyo ( in Japanese ). [Google Scholar]
- 23. ) Nanba , K.Geographic pathology of malignant lymphoma . In“Current Encyclopedia of Pathology 18b ,” ed. Iijima S. , Ishikawa H. , Kageyama K. , Shimamine T. and Mori W. , pp. 153 – 170 ( 1987. ). Nakayama‐Shoten; , Tokyo ( in Japanese ). [Google Scholar]
- 24. ) Freeman , C. , Berg , J. W. and Cutler , S. J.Occurrence and prognosis of extra nodal lymphomas . Cancer , 29 , 252 – 260 ( 1972. ). [DOI] [PubMed] [Google Scholar]
- 25. ) Modan , B. , Shani , M. , Goldman , B. and Modan , M.Nodal and extra nodal lymphoma in Israel: an epidemiological study . Br. J. Haematol. , 16 , 53 – 59 ( 1969. ). [DOI] [PubMed] [Google Scholar]
- 26. ) “Finnish Cancer Registry: Cancer Incidence in Finland 1966 ,” Publ. No. 15 ( 1969. ). Cancer Society of Finland; , Helsinki . [Google Scholar]
- 27. ) Stalsberg , H.Lymphoreticular tumors in Norway and in other European countries . J. Natl. Cancer Inst. , 50 , 1685 – 1702 ( 1973. ). [PubMed] [Google Scholar]
- 28. ) Banfi , A. , Bonadonna , G. , Carnevali , G. , Oldini , C. and Salini , E.Preferential sites of involvement and spread in malignant lymphomas . Eur. J. Cancer , 4 , 319 – 324 ( 1968. ). [DOI] [PubMed] [Google Scholar]
- 29. ) Non‐Hodgkin's Lymphoma Pathologic Classification Project . National Cancer Institute sponsored study of classification of non‐Hodgkin's lymphomas: summary and description of a Working Formulation for clinical usage . Cancer , 49 , 2112 – 2135 ( 1982. ). [DOI] [PubMed] [Google Scholar]
- 30. ) Tajima , K. and Hinuma , Y.Epidemiology of HTLV‐I/II in Japan and the world . In“Gann Monograph on Cancer Research, No. 39: Advances in Adult T‐Cell Leukemia and HTLV‐I Research ,” ed. Takatsuki K. , Himura Y. and Yoshida M. , pp. 129 – 149 ( 1992. ). Japan Scientific Societies Press; , Tokyo . [Google Scholar]
- 31. ) Hanaoka , M.Clinical pathology of adult T cell leukemia . Acta Haematol. Jpn. , 44 , 4120 – 4130 ( 1981. ). [PubMed] [Google Scholar]
- 32. ) Shimoyama , M.Peripheral T‐cell lymphoma in Japan: recent progress . Ann. Oncol. , 2 ( Suppl. 2 ), 157 – 162 ( 1991. ). [DOI] [PubMed] [Google Scholar]
- 33. ) Tajima , K. , Tominaga , S. , Koroishi , T. , Shimizu , H. and Suchi , T.Geographical features and epidemiological approach to endemic T‐cell leukemia/lymphoma in Japan . Jpn. J. Clin. Oncol. , 9 , 495 – 504 ( 1979. ). [Google Scholar]
- 34. ) The T‐ and B‐cell Malignancy Study Group . Statistical analysis of immunologic, clinical and histopathological data on lymphoid malignancies in Japan . Jpn. J. Clin. Oncol. , 11 , 15 – 32 ( 1981. ). [Google Scholar]
- 35. ) Lukes , R. J. , Parker , J. W. , Taylor , C. R. , Tindle , B. H. , Cramer , A. D. and Lincoln , T. L.Immunologic approach to non‐Hodgkin's lymphoma and related leukemias. Analysis of results of multiparameter studies of 425 cases . Semin. Hematol. , 15 , 322 – 351 ( 1978. ). [PubMed] [Google Scholar]
- 36. ) Harris , N. L. , Jaffe , E. S. , Stein , H. , Banks , P. M. , Chan , J. K. C. , Cleary , M. L. , Delsol , G. , De Wolf‐Peeters , C. , Falini , B. , Gatter , K. C. , Grogan , T. M. , Isaacson , P. G. , Knowles , D. M. , Mason , D. Y. , Muller‐Hermelink , H. K. , Pileri , S. A. , Piris , M. A. , Ralfkiaer , E. and Warnke , R. A.Lymphoma classification proposal: clarification . Blood , 85 , 857 – 860 ( 1995. ). [PubMed] [Google Scholar]
- 37. ) Tamaru , J. , Isobe , K. and Mikata , A.REAL classification . Pathol. Clin. Med. , 16 , 399 – 413 ( 1998. ). ( in Japanese ). [Google Scholar]
- 38. ) Kadin , M. E. , Berald , C. W. , Namba , K. and Wakasa , H.Lymphoproliferative diseases in Japan and Western countries . Hum. Pathol. , 14 , 745 – 772 ( 1983. ). [DOI] [PubMed] [Google Scholar]
- 39. ) Warnke , R. A. , Weiss , L. M. , Chan , J. K. C. , Cleary , M. L. and Dorfman , R. F.Malignant lymphoma, follicular . In“Tumors of the Lymph Nodes and Spleen: Atlas of Tumor Pathology, 3rd, Fascicle 14 ,” ed. Rosai J. , pp. 63 – 118 ( 1995. ). A.F.I.P. , Washington , DC . [Google Scholar]
- 40. ) Oyama , A. and Ota , K.Non‐Hodgkin's lymphoma: a clinico‐pathologic study using a new histological classification . Acta Haematol. Jpn. , 44 , 1411 – 1419 ( 1981. ). [PubMed] [Google Scholar]
- 41. ) Katsumata , N. , Matsuno , Y. , Nakayama , H. , Takenaka , T. , Kobayashi , Y. , Takeyama , K. , Narabayashi , M. , Fukushima , T. , Yokozawa , T. , Nakata , M. , Tajima , K. , Ikeda , H. and Tobinai , K.Prognostic factors and a predictive model of follicular lymphoma: a 25‐year study at a single institution in Japan . Jpn. J. Clin. Oncol. , 26 , 445 – 454 ( 1996. ). [DOI] [PubMed] [Google Scholar]
- 42. ) Fifth International Workshop on Chromosomes in Leukemia‐Lymphoma . Correlation of chromosome abnormalities with histologic and immunologic characteristics in non‐Hodgkin's lymphoma and adult T cell leukemia‐lymphoma . Blood , 70 , 1554 – 1564 ( 1987. ). [PubMed] [Google Scholar]
- 43. ) Amakawa , R. , Fukuhara , S. , Ohno , H. , Doi , S. , Oguma , S. , Tanabe , S. , Yamada , H. , Edamura , S. , Tomono , N. , Nasu , K. , Konaka , Y. , Shiomura , T. , Abe , M. , Wakasa , H. and Uchino , H.Involvement of bcl‐2 gene in Japanese follicular lymphoma . Blood , 73 , 787 – 791 ( 1989. ). [PubMed] [Google Scholar]
- 44. ) Greer , J. P. , York , J. C. , Cousar , J. B. , Michell , R. T. , Flexner , J. M. , Collins , R. D. and Stein , R. S.Peripheral Tcell lymphoma: a clinicopathologic study of 42 cases . J. Clin. Oncol. , 2 , 788 – 798 ( 1984. ). [DOI] [PubMed] [Google Scholar]
- 45. ) Jaffe , E. S.Pathologic and clinical spectrum of post‐thymic T‐cell malignancies . Cancer Invest. , 2 , 413 – 426 ( 1984. ). [DOI] [PubMed] [Google Scholar]
- 46. ) Shimoyama , M. , Oyama , A. , Tajima , K. , Tobinai , K. , Minato , K. , Takenaka , T. , Konda , C. , Takeyama , K. , Kohno , A. , Narabayashi , M. , Tamayose , K. , Suzuki , H. , Kurita , S. , Ohta , K. , Mukai , K. , Watanabe , S. and Suchi , T.Differences in clinicopathological characteristics and major prognostic factors between B‐lymphoma and peripheral Tlymphoma excluding adult T‐cell leukemia/lymphoma . Leuk. Lymphoma , 10 , 335 – 342 ( 1993. ). [DOI] [PubMed] [Google Scholar]
- 47. ) Fisher , R. I. , Dahlberg , S. , Nathwani , B. N. , Banks , P. M. , Miller , T. P. and Grogan , T. L.A clinical analysis of two indolent lymphoma entities: mantle cell lymphoma and marginal zone lymphoma (including the mucosa‐associated lymphoid tissue and monocytoid B‐cell subcategories): a Southwest Oncology Group Study . Blood , 85 , 1075 – 1082 ( 1995. ). [PubMed] [Google Scholar]
- 48. ) Shimoyama , M.Treatment of patients with adult T‐cell leukemia‐lymphoma: an overview . In“Gann Monograph on Cancer Research No.39: Advances in Adult T‐Cell Leukemia and HTLV‐1 Research ,” ed. Takatsuki K. , Hinuma Y. and Yoshida M. , pp. 43 – 56 ( 1992. ). Japan Scientific Societies Press; , Tokyo . [Google Scholar]
- 49. ) Kikuchi , M. , Ohshima , K. and Suzumiya , J.Histological spectrum of T‐cell lymphoma in new WHO classification based on REAL classification . Pathol. Clin. Med. , 16 , 384 – 389 ( 1998. ). ( in Japanese ). [Google Scholar]
- 50. ) Izumo , T. , Maseki , N. and Kaneko , Y.An evaluation of REAL classification on malignant lymphoma in Japan . J. Jpn. Soc. Lymphoreticular Tissue Res. , 36 , 145 – 156 ( 1996. ). ( in Japanese ). [Google Scholar]
- 51. ) Kwak , L. W. , Wilson , M. , Weiss , L. M. , Horning , S. J. , Warnke , R. A. and Dorfman , R. F.Clinical significance of morphologic subdivision in diffuse large cell lymphoma . Cancer , 68 , 1988 – 1993 ( 1991. ). [DOI] [PubMed] [Google Scholar]
- 52. ) Engelhard , M. , Brittinger , G. , Huhn , D. , Gerhartz , H. H. , Meusers , P. , Siegert , W. , Thiel , E. , Wilmanns , W. , Aydemir , U. , Bierwolf , S. , Griesser , H. , Tiemann , M. and Lennert , K.Subclassification of diffuse large B‐cell lymphomas according to the Kiel classification: distinction of centroblastic and immunoblastic lymphomas is a significant prognostic risk factor . Blood , 89 , 2291 – 2297 ( 1997. ). [PubMed] [Google Scholar]
- 53. ) Nakamura , S. , Sasaki , K. and Yokoi , T.Large B‐cell lymphoma: its heterogeneity . Pathol. Clin. Med. , 17 , 576 – 581 ( 1999. ). ( in Japanese ). [Google Scholar]
