Skip to main content
PMC home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1983 Nov;113(2):181–197.

Centrocytic lymphoma: a distinct clinicopathologic and immunologic entity. A multiparameter study of 18 cases at diagnosis and relapse.

S H Swerdlow, J A Habeshaw, L J Murray, H S Dhaliwal, T A Lister, A G Stansfeld
PMCID: PMC1916376  PMID: 6416075

Abstract

The clinical, pathologic, and immunologic aspects of malignant lymphoma of centrocytic type (ML,cc) were studied at diagnosis and often at relapse in 18 patients. The typical patient was a middle-aged or older man with adenopathy, often massive splenomegaly, hepatomegaly, marrow involvement, and, not infrequently, peripheral blood involvement. Histopathologically, ML,cc had a diffuse or vaguely nodular growth pattern with, predominantly, cells resembling centrocytes (cleaved follicular center cells) sometimes with admixed small round lymphocytes but with virtually no transformed cells. In 2 cases the neoplastic cells formed a mantle zone around reactive-appearing follicles. Cell suspensions and frozen sections revealed the monoclonal B-cell nature of all but 1 nonmarking case, and the polyclonality of the follicles in the 1 mantle zone case tested. The B cells had some, but not all, characteristics of both normal mantle and follicular center cells when eight nodes were studied with the use of a panel of monoclonal antibodies, peanut lectin, and endogenous alkaline phosphatase activity. Of 13 patients who underwent repeat biopsies, 1 developed a high grade unclassifiable B-cell lymphoma, and 6 had less marked changes. None of 7 patients tested had a change in light chain class. In conclusion, ML,cc is a distinct entity separable from other B-cell lymphomas in which either centrocytes or small round lymphocytes predominate.

Full text

PDF
181

Images in this article

190Figure 6
on p.190
191Figure 7
on p.191
191Figure 8
on p.191
191Figure 9
on p.191
185Figure 1
on p.185
185Figure 2
on p.185
186Figure 3
on p.186
186Figure 4
on p.186

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abo T., Balch C. M. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol. 1981 Sep;127(3):1024–1029. [PubMed] [Google Scholar]
  2. Abramson C. S., Kersey J. H., LeBien T. W. A monoclonal antibody (BA-1) reactive with cells of human B lymphocyte lineage. J Immunol. 1981 Jan;126(1):83–88. [PubMed] [Google Scholar]
  3. Aisenberg A. C., Bloch K. J., Wilkes B. M. Malignant lymphoma with dual B and T cell markers. Analysis of the neoplastic cells with monoclonal antibodies directed against T cell subsets. J Exp Med. 1981 Nov 1;154(5):1709–1714. doi: 10.1084/jem.154.5.1709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bearman R. M., Pangalis G. A., Rappaport H. Prolymphocytic leukemia: clinical, histopathological, and cytochemical observations. Cancer. 1978 Nov;42(5):2360–2372. doi: 10.1002/1097-0142(197811)42:5<2360::aid-cncr2820420537>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
  5. Berard C. W., Jaffe E. S., Braylan R. C., Mann R. B., Nanba K. Immunologic aspects and pathology of the malignant lymphomas. Cancer. 1978 Aug;42(2 Suppl):911–921. doi: 10.1002/1097-0142(197808)42:2+<911::aid-cncr2820420713>3.0.co;2-g. [DOI] [PubMed] [Google Scholar]
  6. Beverley P. C., Callard R. E. Distinctive functional characteristics of human "T" lymphocytes defined by E rosetting or a monoclonal anti-T cell antibody. Eur J Immunol. 1981 Apr;11(4):329–334. doi: 10.1002/eji.1830110412. [DOI] [PubMed] [Google Scholar]
  7. Bhan A. K., Nadler L. M., Stashenko P., McCluskey R. T., Schlossman S. F. Stages of B cell differentiation in human lymphoid tissue. J Exp Med. 1981 Sep 1;154(3):737–749. doi: 10.1084/jem.154.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brittinger G. Outline of a prospective multicentric study on the clinical significance of the Kiel classification of non-Hodgkin's lymphomas. Recent Results Cancer Res. 1978;65:197–202. doi: 10.1007/978-3-642-81249-1_24. [DOI] [PubMed] [Google Scholar]
  9. Caligaris-Cappio F., Gobbi M., Bofill M., Janossy G. Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia. J Exp Med. 1982 Feb 1;155(2):623–628. doi: 10.1084/jem.155.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Charron D. J., McDevitt H. O. Analysis of HLA-D region-associated molecules with monoclonal antibody. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6567–6571. doi: 10.1073/pnas.76.12.6567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cossman J., Jaffe E. S. Distribution of complement receptor subtypes in non-Hodgkin's lymphomas of B-cell origin. Blood. 1981 Jul;58(1):20–26. [PubMed] [Google Scholar]
  12. Costello C., Catovsky D., O'Brien M., Galton D. A. Prolymphocytic leukaemia: an ultrastructural study of 22 cases. Br J Haematol. 1980 Mar;44(3):389–394. doi: 10.1111/j.1365-2141.1980.tb05908.x. [DOI] [PubMed] [Google Scholar]
  13. Cullen M. H., Lister T. A., Brearley R. I., Shand W. S., Stansfeld A. G. Histological transformation of non-Hodgkin's lymphoma: a prospective study. Cancer. 1979 Aug;44(2):645–651. doi: 10.1002/1097-0142(197908)44:2<645::aid-cncr2820440234>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
  14. Evans H. L., Butler J. J., Youness E. L. Malignant lymphoma, small lymphocytic type: a clinicopathologic study of 84 cases with suggested criteria for intermediate lymphocytic lymphoma. Cancer. 1978 Apr;41(4):1440–1455. doi: 10.1002/1097-0142(197804)41:4<1440::aid-cncr2820410432>3.0.co;2-g. [DOI] [PubMed] [Google Scholar]
  15. Foon K. A., Schroff R. W., Gale R. P. Surface markers on leukemia and lymphoma cells: recent advances. Blood. 1982 Jul;60(1):1–19. [PubMed] [Google Scholar]
  16. Galton D. A., Goldman J. M., Wiltshaw E., Catovsky D., Henry K., Goldenberg G. J. Prolymphocytic leukaemia. Br J Haematol. 1974 May;27(1):7–23. doi: 10.1111/j.1365-2141.1974.tb06769.x. [DOI] [PubMed] [Google Scholar]
  17. Gerdes J., Stein H. Immunohistological demonstration and physiochemical characterization of C3 receptors of normal and neoplastic lymphoid cells. J Cancer Res Clin Oncol. 1981;101(1):69–74. doi: 10.1007/BF00405066. [DOI] [PubMed] [Google Scholar]
  18. Godal T., Lindmo T., Ruud E., Heikkilä R., Henriksen A., Steen H. B., Marton P. F. Immunologic subsets in human B-cell lymphomas in relation to normal B-cell development. Haematol Blood Transfus. 1981;26:314–319. doi: 10.1007/978-3-642-67984-1_54. [DOI] [PubMed] [Google Scholar]
  19. Habeshaw J. A., Bailey D., Stansfeld A. G., Greaves M. F. The cellular content of non Hodgkin lymphomas: a comprehensive analysis using monoclonal antibodies and other surface marker techniques. Br J Cancer. 1983 Mar;47(3):327–351. doi: 10.1038/bjc.1983.52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Habeshaw J. A., Catley P. F., Stansfeld A. G., Brearley R. L. Surface phenotyping, histology and the nature of non-Hodgkin lymphoma in 157 patients. Br J Cancer. 1979 Jul;40(1):11–34. doi: 10.1038/bjc.1979.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  22. Jaffe E. S., Braylan R. C., Nanba K., Frank M. M., Berard C. W. Functional markers: a new perspective on malignant lymphomas. Cancer Treat Rep. 1977 Sep;61(6):953–962. [PubMed] [Google Scholar]
  23. Jaffe E. S., Shevach E. M., Frank M. M., Berard C. W., Green I. Nodular lymphoma--evidence for origin from follicular B lymphocytes. N Engl J Med. 1974 Apr 11;290(15):813–819. doi: 10.1056/NEJM197404112901501. [DOI] [PubMed] [Google Scholar]
  24. Katayama I., Aiba M., Pechet L., Sullivan J. L., Roberts P., Humphreys R. E. B-lineage prolymphocytic leukemia as a distinct clinicopathologic entity. Am J Pathol. 1980 May;99(2):399–412. [PMC free article] [PubMed] [Google Scholar]
  25. Kersey J. H., LeBien T. W., Abramson C. S., Newman R., Sutherland R., Greaves M. P-24: a human leukemia-associated and lymphohemopoietic progenitor cell surface structure identified with monoclonal antibody. J Exp Med. 1981 Mar 1;153(3):726–731. doi: 10.1084/jem.153.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kraal G., Weissman I. L., Butcher E. C. Germinal centre B cells: antigen specificity and changes in heavy chain class expression. Nature. 1982 Jul 22;298(5872):377–379. doi: 10.1038/298377a0. [DOI] [PubMed] [Google Scholar]
  27. Ledbetter J. A., Evans R. L., Lipinski M., Cunningham-Rundles C., Good R. A., Herzenberg L. A. Evolutionary conservation of surface molecules that distinguish T lymphocyte helper/inducer and cytotoxic/suppressor subpopulations in mouse and man. J Exp Med. 1981 Feb 1;153(2):310–323. doi: 10.1084/jem.153.2.310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Leech J. H., Glick A. D., Waldron J. A., Flexner J. M., Horn R. G., Collins R. D. Malignant lymphomas of follicular center cell origin in man. I. Immunologic studies. J Natl Cancer Inst. 1975 Jan;54(1):11–21. doi: 10.1093/jnci/54.1.11. [DOI] [PubMed] [Google Scholar]
  29. Lukes R. J., Collins R. D. Immunologic characterization of human malignant lymphomas. Cancer. 1974 Oct;34(4 Suppl):suppl–suppl:1503. doi: 10.1002/1097-0142(197410)34:8+<1488::aid-cncr2820340822>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  30. Lukes R. J., Parker J. W., Taylor C. R., Tindle B. H., Cramer A. D., Lincoln T. L. Immunologic approach to non-Hodgkin lymphomas and related leukemias. Analysis of the results of multiparameter studies of 425 cases. Semin Hematol. 1978 Oct;15(4):322–351. [PubMed] [Google Scholar]
  31. Mann R. B., Jaffe E. S., Berard C. W. Malignant lymphomas--a conceptual understanding of morphologic diversity. A review. Am J Pathol. 1979 Jan;94(1):105–192. [PMC free article] [PubMed] [Google Scholar]
  32. Martin P. J., Hansen J. A., Siadak A. W., Nowinski R. C. Monoclonal antibodies recognizing normal human T lymphocytes and malignant human B lymphocytes: a comparative study. J Immunol. 1981 Nov;127(5):1920–1923. [PubMed] [Google Scholar]
  33. Meugé C., Hoerni B., de Mascarel A., Durand M., Richaud P., Hoerni-Simon G., Chauvergne J., Lagarde C. Non-Hodgkin malignant lymphomas. Clinico-pathologic correlations with the Kiel classification. Retrospective analysis of a series of 274 cases. Eur J Cancer. 1978 May;14(5):587–592. doi: 10.1016/0014-2964(78)90263-3. [DOI] [PubMed] [Google Scholar]
  34. Nadler L. M., Ritz J., Hardy R., Pesando J. M., Schlossman S. F., Stashenko P. A unique cell surface antigen identifying lymphoid malignancies of B cell origin. J Clin Invest. 1981 Jan;67(1):134–140. doi: 10.1172/JCI110005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Nanba K., Jaffe E. S., Braylan R. C., Soban E. J., Berard C. W. Alkaline phosphatase-positive malignant lymphoma. A subtype of B-cell lymphomas. Am J Clin Pathol. 1977 Nov;68(5):535–542. doi: 10.1093/ajcp/68.5.535. [DOI] [PubMed] [Google Scholar]
  36. Nieuwenhuis P., Gastkemper N. A., Opstelten D. Histophysiology of follicular structures and germinal centres in relation to B cell differentiation. Ciba Found Symp. 1981;84:246–264. doi: 10.1002/9780470720660.ch13. [DOI] [PubMed] [Google Scholar]
  37. Pallesen G., Madsen M., Pedersen B. B. B-prolymphocytic leukaemia--a mantle zone lymphoma? Scand J Haematol. 1979 May;22(5):407–416. doi: 10.1111/j.1600-0609.1979.tb00438.x. [DOI] [PubMed] [Google Scholar]
  38. Palutke M., Eisenberg L., Mirchandani I., Tabaczka P., Husain M. Malignant lymphoma of small cleaved lymphocytes of the follicular mantle zone. Blood. 1982 Feb;59(2):317–322. [PubMed] [Google Scholar]
  39. Parker J. W. Immunologic basis for the redefinition of malignant lymphomas. Am J Clin Pathol. 1979 Oct;72(4 Suppl):670–686. [PubMed] [Google Scholar]
  40. Peto R., Pike M. C., Armitage P., Breslow N. E., Cox D. R., Howard S. V., Mantel N., McPherson K., Peto J., Smith P. G. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. analysis and examples. Br J Cancer. 1977 Jan;35(1):1–39. doi: 10.1038/bjc.1977.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pinkus G. S., Said J. W. Characterization of non-Hodgkin's lymphomas using multiple cell markers. Immunologic, morphologic, and cytochemical studies of 72 cases. Am J Pathol. 1979 Feb;94(2):349–380. [PMC free article] [PubMed] [Google Scholar]
  42. Poppema S., Elema J. D., Halie M. R. Alkaline phosphatase positive lymphomas: a morphologic, immunologic, and enzymehistochemical study. Cancer. 1981 Mar 15;47(6):1303–1312. doi: 10.1002/1097-0142(19810315)47:6<1303::aid-cncr2820470612>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
  43. Ritz J., Nadler L. M., Bhan A. K., Notis-McConarty J., Pesando J. M., Schlossman S. F. Expression of common acute lymphoblastic leukemia antigen (CALLA) by lymphomas of B-cell and T-cell lineage. Blood. 1981 Sep;58(3):648–652. [PubMed] [Google Scholar]
  44. Rose M. L., Habeshaw J. A., Kennedy R., Sloane J., Wiltshaw E., Davies A. J. Binding of peanut lectin to germinal-centre cells: a marker for B-cell subsets of follicular lymphoma? Br J Cancer. 1981 Jul;44(1):68–74. doi: 10.1038/bjc.1981.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Royston I., Majda J. A., Baird S. M., Meserve B. L., Griffiths J. C. Human T cell antigens defined by monoclonal antibodies: the 65,000-dalton antigen of T cells (T65) is also found on chronic lymphocytic leukemia cells bearing surface immunoglobulin. J Immunol. 1980 Aug;125(2):725–731. [PubMed] [Google Scholar]
  46. Schroff R. W., Foon K. A., Billing R. J., Fahey J. L. Immunologic classification of lymphocytic leukemias based on monoclonal antibody-defined cell surface antigens. Blood. 1982 Feb;59(2):207–215. [PubMed] [Google Scholar]
  47. Stein H., Bonk A., Tolksdorf G., Lennert K., Rodt H., Gerdes J. Immunohistologic analysis of the organization of normal lymphoid tissue and non-Hodgkin's lymphomas. J Histochem Cytochem. 1980 Aug;28(8):746–760. doi: 10.1177/28.8.7003001. [DOI] [PubMed] [Google Scholar]
  48. Stein H., Gerdes J., Mason D. Y. The normal and malignant germinal centre. Clin Haematol. 1982 Oct;11(3):531–559. [PubMed] [Google Scholar]
  49. Stein H., Staudinger M., Tolksdorf G., Lennert K. Immunologic markers in the differential diagnosis of non-Hodgkin's lymphomas. J Cancer Res Clin Oncol. 1981;101(1):29–42. doi: 10.1007/BF00405061. [DOI] [PubMed] [Google Scholar]
  50. Tolksdorf G., Stein H., Lennert K. Morphological and immunological definition of a malignant lymphoma derived from germinal-centre cells with cleaved nuclei (centrocytes). Br J Cancer. 1980 Feb;41(2):168–182. doi: 10.1038/bjc.1980.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Verbi W., Greaves M. F., Schneider C., Koubek K., Janossy G., Stein H., Kung P., Goldstein G. Monoclonal antibodies OKT 11 and OKT 11A have pan-T reactivity and block sheep erythrocyte "receptors". Eur J Immunol. 1982 Jan;12(1):81–86. doi: 10.1002/eji.1830120115. [DOI] [PubMed] [Google Scholar]
  52. Weisenburger D. D., Kim H., Rappaport H. Mantle-zone lymphoma: a follicular variant of intermediate lymphocytic lymphoma. Cancer. 1982 Apr 1;49(7):1429–1438. doi: 10.1002/1097-0142(19820401)49:7<1429::aid-cncr2820490720>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  53. Weisenburger D. D., Nathwani B. N., Diamond L. W., Winberg C. D., Rappaport H. Malignant lymphoma, intermediate lymphocytic type: a clinicopathologic study of 42 cases. Cancer. 1981 Sep 15;48(6):1415–1425. doi: 10.1002/1097-0142(19810915)48:6<1415::aid-cncr2820480625>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  54. Yu D. T., Winchester R. J., Fu S. M., Gibofsky A., Ko H. S., Kunkel H. G. Peripheral blood Ia-positive T cells. Increases in certain diseases and after immunization. J Exp Med. 1980 Jan 1;151(1):91–100. doi: 10.1084/jem.151.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES