Skip to main content
Journal of Clinical Pathology logoLink to Journal of Clinical Pathology
. 1984 Mar;37(3):233–254. doi: 10.1136/jcp.37.3.233

Lymphoproliferations in the bone marrow: identification and evolution, classification and staging.

R Bartl, B Frisch, R Burkhardt, K Jäger, R Pappenberger, G Hoffmann-Fezer
PMCID: PMC498694  PMID: 6699189

Abstract

Bone marrow biopsies from 3229 patients with lymphoproliferative disorders and 1156 patients with benign or reactive lymphoproliferations were investigated and criteria for distinguishing between them are given. Bone marrow involvement was found in 89% of multiple myeloma, 64% of non-Hodgkin's lymphomas and 8% of Hodgkin's disease. According to the predominant proliferative cell type there were five major entities in multiple myeloma and non-Hodgkin's lymphomas: (1) plasmacytic; (2) lymphocytic; (3) hairy cell; (4) immunocytic; (5) centrocytic. These were further classified into distinct subtypes each of which had independent prognostic significance. The mode of spread of the lymphoproliferative disorders in the bone marrow showed one of six architectural patterns, which together with the quantity of infiltration in the biopsy (reflecting the tumour cell burden) had significant predictive value. These results demonstrate the value of bone marrow biopsies in the identification, classification and staging of lymphoproliferative disorders, as well as in monitoring the course of disease and the response to therapy.

Full text

PDF
233

Images in this article

Selected References

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

  1. Aisenberg A. C. Cell lineage in lymphoproliferative disease. Am J Med. 1983 Apr;74(4):679–685. doi: 10.1016/0002-9343(83)91027-6. [DOI] [PubMed] [Google Scholar]
  2. Baccarani M., Cavo M., Gobbi M., Lauria F., Tura S. Staging of chronic lymphocytic leukemia. Blood. 1982 Jun;59(6):1191–1196. [PubMed] [Google Scholar]
  3. Bain G. O. Non-Hodgkin's lymphomas. Analysis of 92 cases using the 'international' classification. Arch Pathol Lab Med. 1983 Feb;107(2):64–69. [PubMed] [Google Scholar]
  4. Barcos M., Herrmann R., Pickren J. W., Naeher C., Han T., Stutzman L., Henderson E. S. The influence of histologic type on survival in non-Hodgkin's lymphoma. Cancer. 1981 Jun 15;47(12):2894–2900. doi: 10.1002/1097-0142(19810615)47:12<2894::aid-cncr2820471224>3.0.co;2-8. [DOI] [PubMed] [Google Scholar]
  5. Bartl R., Burkhardt R., Gierster P., Sandel P., Fateh-Moghadam A. Significance of bone marrow biopsy in the multiple myeloma. Bibl Haematol. 1978;45:81–86. doi: 10.1159/000402187. [DOI] [PubMed] [Google Scholar]
  6. Bartl R., Burkhardt R., Vondracek H., Sommerfeld W., Hagemeister E. Rationelle Beckenkamm-Biopsie Längsteilung der Proben zur Anwendung von mehreren Präparationsverfahren ohne Materialverlust. Klin Wochenschr. 1978 Jun 1;56(11):545–550. doi: 10.1007/BF01477250. [DOI] [PubMed] [Google Scholar]
  7. Bartl R., Frisch B., Burkhardt R., Hoffmann-Fezer G., Demmler K., Sund M. Assessment of marrow trephine in relation to staging in chronic lymphocytic leukaemia. Br J Haematol. 1982 May;51(1):1–15. doi: 10.1111/j.1365-2141.1982.tb07284.x. [DOI] [PubMed] [Google Scholar]
  8. Bartl R., Frisch B., Burkhardt R., Huhn D., Pappenberger R. Assessment of bone marrow histology in Hodgkin's disease: correlation with clinical factors. Br J Haematol. 1982 Jul;51(3):345–360. doi: 10.1111/j.1365-2141.1982.tb02790.x. [DOI] [PubMed] [Google Scholar]
  9. Bartl R., Frisch B., Burkhardt R., Kettner G., Mahl G., Fateh-Moghadam A., Sund M. Assessment of bone marrow histology in the malignant lymphomas (non-Hodgkin's): correlation with clinical factors for diagnosis, prognosis, classification and staging. Br J Haematol. 1982 Aug;51(4):511–530. doi: 10.1111/j.1365-2141.1982.tb02815.x. [DOI] [PubMed] [Google Scholar]
  10. Bartl R., Frisch B., Hill W., Burkhardt R., Sommerfeld W., Sund M. Bone marrow histology in hairy cell leukemia. Identification of subtypes and their prognostic significance. Am J Clin Pathol. 1983 May;79(5):531–545. doi: 10.1093/ajcp/79.5.531. [DOI] [PubMed] [Google Scholar]
  11. Bartl R., Frisch B., Mahl G., Burkhardt R., Fateh-Moghadam A., Pappenberger R., Sommerfeld W., Hoffmann-Fezer G. Bone marrow histology in Waldenström's macroglobulinaemia. Clinical relevance of subtype recognition. Scand J Haematol. 1983 Oct;31(4):359–375. doi: 10.1111/j.1600-0609.1983.tb00664.x. [DOI] [PubMed] [Google Scholar]
  12. Barton J. C., Conrad M. E., Vogler L. B., Parmley R. T. Isolated marrow lymphoma: an entity of possible T-cell derivation. Cancer. 1980 Oct 15;46(8):1767–1774. doi: 10.1002/1097-0142(19801015)46:8<1767::aid-cncr2820460812>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  13. Bergsagel D. E. Plasma cell neoplasms and acute leukaemia. Clin Haematol. 1982 Feb;11(1):221–234. [PubMed] [Google Scholar]
  14. Berrebi A., Talmor M., Vorst E., Resnitzky P., Shtalrid M. IgM lambda globular cytoplasmic inclusions in chronic lymphocytic leukaemia resembling immunocytoma. Scand J Haematol. 1983 Jan;30(1):43–49. doi: 10.1111/j.1600-0609.1983.tb00633.x. [DOI] [PubMed] [Google Scholar]
  15. Bettini R., Chelazzi G. Prognostic value of the Kiel classification of malignant non-Hodgkin's lymphomas. Tumori. 1979 Apr 30;65(2):207–213. doi: 10.1177/030089167906500209. [DOI] [PubMed] [Google Scholar]
  16. Bluming A. Z., Cohen H. G., Saxon A. Angioimmunoblastic lymphadenopathy with dysproteinemia. A pathogenetic link between lymphoid proliferation and malignant lymphoma. Am J Med. 1979 Sep;67(3):421–428. doi: 10.1016/0002-9343(79)90788-5. [DOI] [PubMed] [Google Scholar]
  17. Brunning R. D., McKenna R. W. Bone marrow manifestations of malignant lymphoma and lymphoma-like conditions. Pathol Annu. 1979;14(Pt 1):1–59. [PubMed] [Google Scholar]
  18. Buckman R., Cuzick J., Galton D. A. Long-term survival in myelomatosis. A report to the MRC working party on leukaemia in adults. Br J Haematol. 1982 Dec;52(4):589–599. doi: 10.1111/j.1365-2141.1982.tb03935.x. [DOI] [PubMed] [Google Scholar]
  19. Burkhardt R., Frisch B., Bartl R. Bone biopsy in haematological disorders. J Clin Pathol. 1982 Mar;35(3):257–284. doi: 10.1136/jcp.35.3.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Canioni D., Kermarec J. Interprétation des plasmocytoses médullaires minimes dans les dysglobulinémies monoclonales. Intérêt de l'étude de biopsies ostéomédullaires sur coupes semi-fines et par marquage immunologique. Ann Pathol. 1982;2(4):279–292. [PubMed] [Google Scholar]
  21. Carbone A., Santoro A., Pilotti S., Rilke F. Bone-marrow patterns and clinical staging in chronic lymphocytic leukaemia. Lancet. 1978 Mar 18;1(8064):606–606. doi: 10.1016/s0140-6736(78)91048-6. [DOI] [PubMed] [Google Scholar]
  22. Charron D., Dighiero G., Raphael M., Binet J. L. Bone-marrow patterns and clinical staging in chronic lymphocyte leukaemia. Lancet. 1977 Oct 15;2(8042):819–819. doi: 10.1016/s0140-6736(77)90751-6. [DOI] [PubMed] [Google Scholar]
  23. Child J. A., Crawford S. M., Norfolk D. R., O'Quigley J., Scarffe J. H., Struthers L. P. Evaluation of serum beta 2-microglobulin as a prognostic indicator in myelomatosis. Br J Cancer. 1983 Jan;47(1):111–114. doi: 10.1038/bjc.1983.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Damber L., Lenner P., Lundgren E. The impact of growth pattern on survival in non-Hodgkin's lymphomas classified according to Lukes and Collins. Pathol Res Pract. 1982 Jul;174(1-2):42–52. doi: 10.1016/S0344-0338(82)80027-7. [DOI] [PubMed] [Google Scholar]
  26. Dardick I., Setterfield G., Hall R., Bladon T., Little J., Kaplan G. Nuclear alterations during lymphocyte transformation: relationship to the heterogeneous morphologic presentations of non-Hodgkin's lymphomas. Am J Pathol. 1981 Apr;103(1):10–20. [PMC free article] [PubMed] [Google Scholar]
  27. Demanes D. J., Lane N., Beckstead J. H. Bone involvement in hairy-cell leukemia. Cancer. 1982 Apr 15;49(8):1697–1701. doi: 10.1002/1097-0142(19820415)49:8<1697::aid-cncr2820490826>3.0.co;2-0. [DOI] [PubMed] [Google Scholar]
  28. Dosoretz D. E., Raymond A. K., Murphy G. F., Doppke K. P., Schiller A. L., Wang C. C., Suit H. D. Primary lymphoma of bone: the relationship of morphologic diversity to clinical behavior. Cancer. 1982 Sep 1;50(5):1009–1014. doi: 10.1002/1097-0142(19820901)50:5<1009::aid-cncr2820500532>3.0.co;2-0. [DOI] [PubMed] [Google Scholar]
  29. Durie B. G., Salmon S. E., Moon T. E. Pretreatment tumor mass, cell kinetics, and prognosis in multiple myeloma. Blood. 1980 Mar;55(3):364–372. [PubMed] [Google Scholar]
  30. Economopoulos T., Fotopoulos S., Hatzioannou J., Gardikas C. 'Prolymphocytoid' cells in chronic lymphocytic leukaemia and their prognostic significance. Scand J Haematol. 1982 Mar;28(3):238–242. doi: 10.1111/j.1600-0609.1982.tb00521.x. [DOI] [PubMed] [Google Scholar]
  31. Falini B., De Solas I., Levine A. M., Parker J. W., Lukes R. J., Taylor C. R. Emergence of B-immunoblastic sarcoma in patients with multiple myeloma: a clinicopathologic study of 10 cases. Blood. 1982 May;59(5):923–933. [PubMed] [Google Scholar]
  32. Fine J. M., Lambin P., Massari M., Leroux P. Malignant evolution of asymptomatic monoclonal IgM after seven and fifteen years in two siblings of a patient with Waldenström's macroglobulinemia. Acta Med Scand. 1982 May;211(3):237–239. doi: 10.1111/j.0954-6820.1982.tb01935.x. [DOI] [PubMed] [Google Scholar]
  33. Fisher R. I., Jones R. B., DeVita V. T., Jr, Simon R. M., Garvin A. J., Berard C. W., Young R. C. Natural history of malignant lymphomas with divergent histologies at staging evaluation. Cancer. 1981 Apr 15;47(8):2022–2025. doi: 10.1002/1097-0142(19810415)47:8<2022::aid-cncr2820470820>3.0.co;2-v. [DOI] [PubMed] [Google Scholar]
  34. Foucar K., McKenna R. W., Frizzera G., Brunning R. D. Bone marrow and blood involvement by lymphoma in relationship to the Lukes--Collins classification. Cancer. 1982 Mar 1;49(5):888–897. doi: 10.1002/1097-0142(19820301)49:5<888::aid-cncr2820490512>3.0.co;2-k. [DOI] [PubMed] [Google Scholar]
  35. Foucar K., McKenna R. W., Frizzera G., Brunning R. D. Incidence and patterns of bone marrow and blood involvement by lymphoma in relationship to the Lukes-Collins classification. Blood. 1979 Dec;54(6):1417–1422. [PubMed] [Google Scholar]
  36. Frisch B., Bartl R., Burkhardt R. Bone marrow biopsy in clinical medicine: an overview. Haematologia (Budap) 1982;15(3):245–285. [PubMed] [Google Scholar]
  37. 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]
  38. Geisler C., Hansen M. M. Chronic lymphocytic leukaemia: a test of a proposed new clinical staging system. Scand J Haematol. 1981 Oct;27(4):279–286. doi: 10.1111/j.1600-0609.1981.tb00485.x. [DOI] [PubMed] [Google Scholar]
  39. Glimelius B., Hagberg H., Sundström C. Morphological classification of non-Hodgkin malignant lymphoma. II. Comparison between Rappaport's classification and the Kiel classification. Scand J Haematol. 1983 Jan;30(1):13–24. doi: 10.1111/j.1600-0609.1983.tb00629.x. [DOI] [PubMed] [Google Scholar]
  40. Goffinet D. R., Warnke R., Dunnick N. R., Castellino R., Glatstein E., Nelsen T. S., Dorfman R. F., Rosenberg S. A., Kaplan H. S. Clinical and surgical (laparotomy) evaluation of patients with non-Hodgkin's lymphomas. Cancer Treat Rep. 1977 Sep;61(6):981–992. [PubMed] [Google Scholar]
  41. Goldin A., Schabel F. M. Clinical concepts derived from animal chemotherapy studies. Cancer Treat Rep. 1981;65 (Suppl 3):11–19. [PubMed] [Google Scholar]
  42. Gordon D. S., Jones B. M., Browning S. W., Spira T. J., Lawrence D. N. Persistent polyclonal lymphocytosis of B lymphocytes. N Engl J Med. 1982 Jul 22;307(4):232–236. doi: 10.1056/NEJM198207223070407. [DOI] [PubMed] [Google Scholar]
  43. Gray J. L., Jacobs A., Block M. Bone marrow and peripheral blood lymphocytosis in the prognosis of chronic lymphocytic leukemia. Cancer. 1974 Apr;33(4):1169–1178. doi: 10.1002/1097-0142(197404)33:4<1169::aid-cncr2820330441>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
  44. Greenberg B. R., Miller C., Cardiff R. D., MacKenzie M. R., Walling P. Concurrent development of preleukaemic, lymphoproliferative and plasma cell disorders. Br J Haematol. 1983 Jan;53(1):125–133. doi: 10.1111/j.1365-2141.1983.tb01994.x. [DOI] [PubMed] [Google Scholar]
  45. Grossi C. E., Zicca A., Leprini A., Cadoni A., Pistoia V., Ferrarini M. Acid hydrolases as markers of maturation in B-cell chronic lymphocytic leukemia. Blood. 1982 Jul;60(1):220–227. [PubMed] [Google Scholar]
  46. 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]
  47. Han T., Ozer H., Bloom M., Sagawa K., Minowada J. The presence of monoclonal cytoplasmic immunoglobulins in leukemic B cells from patients with chronic lymphocytic leukemia. Blood. 1982 Feb;59(2):435–438. [PubMed] [Google Scholar]
  48. Hernandez-Nieto L., Montserrat-Costa E., Muncunill J., Rozman C. Bone-marrow patterns and clinical staging in chronic lymphocytic leukaemia. Lancet. 1977 Jun 11;1(8024):1269–1269. doi: 10.1016/s0140-6736(77)92489-8. [DOI] [PubMed] [Google Scholar]
  49. Herrmann R., Barcos M., Stutzman L., Walsh D., Freeman A., Sokal J., Henderson E. S. The influence of histologic type on the incidence and duration of response in non-Hodgkin's lymphoma. Cancer. 1982 Jan 15;49(2):314–322. doi: 10.1002/1097-0142(19820115)49:2<314::aid-cncr2820490218>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  50. Hoffmann-Fezer G., Thierfelder S., Pielsticker K., Rodt H. Immunohistochemical demonstration of cell surface antigens on tissue sections of lymphomas. Leuk Res. 1979;3(5):297–304. doi: 10.1016/0145-2126(79)90056-0. [DOI] [PubMed] [Google Scholar]
  51. Hubbard S. M., Chabner B. A., DeVita V. T., Jr, Simon R., Berard C. W., Jones R. B., Garvin A. J., Canellos G. P., Osborne C. K., Young R. C. Histologic progression in non-Hodgkin's lymphoma. Blood. 1982 Feb;59(2):258–264. [PubMed] [Google Scholar]
  52. Hubbard S. M., Chabner B. A., DeVita V. T., Jr, Simon R., Berard C. W., Jones R. B., Garvin A. J., Canellos G. P., Osborne C. K., Young R. C. Histologic progression in non-Hodgkin's lymphoma. Blood. 1982 Feb;59(2):258–264. [PubMed] [Google Scholar]
  53. Jacobsen N., Theilade K., Videbaek A. Two additional cases of coexisting polycythaemia vera and chronic lymphocytic leukaemia. Scand J Haematol. 1982 Nov;29(5):405–410. doi: 10.1111/j.1600-0609.1982.tb00615.x. [DOI] [PubMed] [Google Scholar]
  54. Jacquillat C., Auclerc G., Auclerc M. F., Andrieu J. M., Weil M., Bernard J. Maladie de Hodgkin: caractéristiques et pronostic des formes avec atteinte médullaire initiale. Nouv Presse Med. 1981 Jan 17;10(2):95–100. [PubMed] [Google Scholar]
  55. Jamshidi K., Swaim W. R. Bone marrow biopsy with unaltered architecture: a new biopsy device. J Lab Clin Med. 1971 Feb;77(2):335–342. [PubMed] [Google Scholar]
  56. Jansen J., Hermans J. Clinical staging system for hairy-cell leukemia. Blood. 1982 Sep;60(3):571–577. [PubMed] [Google Scholar]
  57. Jennette J. C., Reddick R. L., Saunders A. W., Wilkman A. S. Diffuse T-cell lymphoma preceded by nodular lymphoma. Am J Clin Pathol. 1982 Aug;78(2):242–248. doi: 10.1093/ajcp/78.2.242. [DOI] [PubMed] [Google Scholar]
  58. Jones S. E., Rosenberg S. A., Kaplan H. S. Non-Hodgkin's lymphomas. I. Bone marrow involvement. Cancer. 1972 Apr;29(4):954–960. doi: 10.1002/1097-0142(197204)29:4<954::aid-cncr2820290442>3.0.co;2-5. [DOI] [PubMed] [Google Scholar]
  59. Kaplan H. S. Hodgkin's disease: unfolding concepts concerning its nature, management and prognosis. Cancer. 1980 May 15;45(10):2439–2474. doi: 10.1002/1097-0142(19800515)45:10<2439::aid-cncr2820451003>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
  60. Kim H., Hendrickson R., Dorfman R. F. Composite lymphoma. Cancer. 1977 Sep;40(3):959–976. doi: 10.1002/1097-0142(197709)40:3<959::aid-cncr2820400302>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
  61. Kyle R. A. Long-term survival in multiple myeloma. N Engl J Med. 1983 Feb 10;308(6):314–316. doi: 10.1056/NEJM198302103080604. [DOI] [PubMed] [Google Scholar]
  62. Latreille J., Barlogie B., Johnston D., Drewinko B., Alexanian R. Ploidy and proliferative characteristics in monoclonal gammopathies. Blood. 1982 Jan;59(1):43–51. [PubMed] [Google Scholar]
  63. Leonard R. C., Cuzick J., MacLennan I. C., Vanhegan R. I., Mackie P. H., McCormick C. V. Prognostic factors in non-Hodgkin's lymphoma: the importance of symptomatic stage as an adjunct to the Kiel histopathological classification. Br J Cancer. 1983 Jan;47(1):91–102. doi: 10.1038/bjc.1983.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Leyser S., Variakojis D., Mintz U., Vardiman J. W., Ultmann J. E. Multiple histologic subtypes of non-Hodgkin's lymphoma: clinical and pathologic features. Cancer. 1981 Nov 1;48(9):2063–2069. doi: 10.1002/1097-0142(19811101)48:9<2063::aid-cncr2820480924>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
  65. Lipshutz M. D., Mir R., Rai K. R., Sawitsky A. Bone marrow biopsy and clinical staging in chronic lymphocytic leukemia. Cancer. 1980 Sep 15;46(6):1422–1427. doi: 10.1002/1097-0142(19800915)46:6<1422::aid-cncr2820460623>3.0.co;2-b. [DOI] [PubMed] [Google Scholar]
  66. Lukes R. J., Tindle B. H. Immunoblastic lymphadenopathy. A hyperimmune entity resembling Hodgkin's disease. N Engl J Med. 1975 Jan 2;292(1):1–8. doi: 10.1056/NEJM197501022920101. [DOI] [PubMed] [Google Scholar]
  67. 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]
  68. Myers C. E., Chabner B. A., De Vita V. T., Gralnick H. R. Bone marrow involvement in Hodgkin's disease: pathology and response to MOPP chemotherapy. Blood. 1974 Aug;44(2):197–204. [PubMed] [Google Scholar]
  69. Nathwani B. N., Kim H., Rappaport H., Solomon J., Fox M. Non-Hodgkin's lymphomas: a clinicopathologic study comparing two classifications. Cancer. 1978 Jan;41(1):303–325. doi: 10.1002/1097-0142(197801)41:1<303::aid-cncr2820410142>3.0.co;2-g. [DOI] [PubMed] [Google Scholar]
  70. O'Carroll D. I., McKenna R. W., Brunning R. D. Bone marrow manifestations of Hodgkin's disease. Cancer. 1976 Oct;38(4):1717–1728. doi: 10.1002/1097-0142(197610)38:4<1717::aid-cncr2820380445>3.0.co;2-9. [DOI] [PubMed] [Google Scholar]
  71. Ostrow S. S., Diggs C. H., Sutherland J. C., Gustafson J., Wiernik P. H. Nodular poorly differentiated lymphocytic lymphoma: changes in histology and survival. Cancer Treat Rep. 1981 Nov-Dec;65(11-12):929–933. [PubMed] [Google Scholar]
  72. Pangalis G. A., Moran E. M., Rappaport H. Blood and bone marrow findings in angioimmunoblastic lymphadenopathy. Blood. 1978 Jan;51(1):71–83. [PubMed] [Google Scholar]
  73. Paterson A. D., Kanis J. A., Cameron E. C., Douglas D. L., Beard D. J., Preston F. E., Russell R. G. The use of dichloromethylene diphosphonate for the management of hypercalcaemia in multiple myeloma. Br J Haematol. 1983 May;54(1):121–132. doi: 10.1111/j.1365-2141.1983.tb02074.x. [DOI] [PubMed] [Google Scholar]
  74. Pennec Y., Mottier D., Youinou P., Asselain B., Chavance M., Le Goff P., Le Prise P. Y., Miossec P., Le Menn G. Critical study of staging in multiple myeloma. Scand J Haematol. 1983 Feb;30(2):183–190. doi: 10.1111/j.1600-0609.1983.tb01468.x. [DOI] [PubMed] [Google Scholar]
  75. Pettersson D., Mellstedt H., Holm G., Bjorkholm M. Monoclonal blood lymphocytes in benign monoclonal gammopathy and multiple myeloma in relation to clinical stage. Scand J Haematol. 1981 Oct;27(4):287–293. doi: 10.1111/j.1600-0609.1981.tb00486.x. [DOI] [PubMed] [Google Scholar]
  76. Pizzolo G., Chilosi M., Cetto G. L., Fiore-Donati L., Janossy G. Immuno-histological analysis of bone marrow involvement in lymphoproliferative disorders. Br J Haematol. 1982 Jan;50(1):95–100. doi: 10.1111/j.1365-2141.1982.tb01894.x. [DOI] [PubMed] [Google Scholar]
  77. Ralfkiaer E., Geisler C., Hansen M. M., Hou-Jensen K. Nuclear clefts in chronic lymphocytic leukaemia. A light microscopic and ultrastructural study of a new prognostic parameter. Scand J Haematol. 1983 Jan;30(1):5–12. doi: 10.1111/j.1600-0609.1983.tb00628.x. [DOI] [PubMed] [Google Scholar]
  78. Redmond J., 3rd, Stites D. P., Beckstead J. H., George C. B., Casavant C. H., Gandara D. R. Chronic lymphocytic leukemia with osteolytic bone lesions, hypercalcemia, and monoclonal protein. Am J Clin Pathol. 1983 May;79(5):616–620. doi: 10.1093/ajcp/79.5.616. [DOI] [PubMed] [Google Scholar]
  79. Rilke F., Pilotti S., Carbone A., Lombardi L. Morphology of lymphatic cells and of their derived tumours. J Clin Pathol. 1978 Nov;31(11):1009–1056. doi: 10.1136/jcp.31.11.1009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Rosenberg S. A. Bone marrow involvement in the non-Hodgkin's lymphomata. Br J Cancer Suppl. 1975 Mar;2:261–264. [PMC free article] [PubMed] [Google Scholar]
  81. Rosenberg S. A., Dorfman R. F., Kaplan H. S. The value of sequential bone marrow biopsy and laparotomy and splenectomy in a series of 127 consecutive untreated patients with non-Hodgkin's lymphoma. Br J Cancer Suppl. 1975 Mar;2:221–227. [PMC free article] [PubMed] [Google Scholar]
  82. Rosenberg S. A. Hodgkin's disease of the bone marrow. Cancer Res. 1971 Nov;31(11):1733–1736. [PubMed] [Google Scholar]
  83. Rowan R. M. Multiple myeloma: some recent developments. Clin Lab Haematol. 1982;4(3):211–230. doi: 10.1111/j.1365-2257.1982.tb00071.x. [DOI] [PubMed] [Google Scholar]
  84. Rozman C., Hernandez-Nieto L., Montserrat E., Brugues R. Prognostic significance of bone-marrow patterns in chronic lymphocytic leukaemia. Br J Haematol. 1981 Apr;47(4):529–537. doi: 10.1111/j.1365-2141.1981.tb02681.x. [DOI] [PubMed] [Google Scholar]
  85. Rywlin A. M., Ortega R. S., Dominguez C. J. Lymphoid nodules of bone marrow: normal and abnormal. Blood. 1974 Mar;43(3):389–400. [PubMed] [Google Scholar]
  86. Schauer P. K., Straus D. J., Bagley C. M., Jr, Rudolph R. H., McCracken J. D., Huff J., Glucksburg H., Bauermeister D. E., Clarkson B. D. Angioimmunoblastic lymphadenopathy: clinical spectrum of disease. Cancer. 1981 Dec 1;48(11):2493–2498. doi: 10.1002/1097-0142(19811201)48:11<2493::aid-cncr2820481124>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
  87. Schnaidt U., Vykoupil K. F., Thiele J., Georgii A. Angioimmunoblastic lymphadenopathy. Histopathology of bone marrow involvement. Virchows Arch A Pathol Anat Histol. 1980;389(3):369–380. doi: 10.1007/BF00430660. [DOI] [PubMed] [Google Scholar]
  88. Skinnider L. F., Tan L., Schmidt J., Armitage G. Chronic lymphocytic leukemia. A review of 745 cases and assessment of clinical staging. Cancer. 1982 Dec 15;50(12):2951–2955. doi: 10.1002/1097-0142(19821215)50:12<2951::aid-cncr2820501241>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
  89. Spagnolo D. V., Papadimitriou J. M., Matz L. R., Walters M. N. Nodular lymphomas with intracellular immunoglobulin inclusions: report of three cases and a review. Pathology. 1982 Oct;14(4):415–427. doi: 10.3109/00313028209092121. [DOI] [PubMed] [Google Scholar]
  90. Stern N., Shemesh J., Ramot B. Chronic lymphatic leukemia terminating in acute myeloid leukemia: review of the literature. Cancer. 1981 Apr 1;47(7):1849–1851. doi: 10.1002/1097-0142(19810401)47:7<1849::aid-cncr2820470722>3.0.co;2-x. [DOI] [PubMed] [Google Scholar]
  91. Straus D. J., Filippa D. A., Lieberman P. H., Koziner B., Thaler H. T., Clarkson B. D. The non-Hodgkin's lymphomas. I. A retrospective clinical and pathologic analysis of 499 cases diagnosed between 1958 and 1969. Cancer. 1983 Jan 1;51(1):101–109. doi: 10.1002/1097-0142(19830101)51:1<101::aid-cncr2820510121>3.0.co;2-w. [DOI] [PubMed] [Google Scholar]
  92. Suchman A. L., Coleman M., Mouradian J. A., Wolf D. J., Saletan S. Aggressive plasma cell myeloma. A terminal phase. Arch Intern Med. 1981 Sep;141(10):1315–1320. [PubMed] [Google Scholar]
  93. Valentin-Opran A., Charhon S. A., Meunier P. J., Edouard C. M., Arlot M. E. Quantitative histology of myeloma-induced bone changes. Br J Haematol. 1982 Dec;52(4):601–610. doi: 10.1111/j.1365-2141.1982.tb03936.x. [DOI] [PubMed] [Google Scholar]
  94. Vercelli D., Di Guglielmo R., Guidi G., Scolari L., Buricchi L., Cozzolino F. Bone marrow percentage of plasma cells in the staging of monoclonal gammopathies. Nouv Rev Fr Hematol. 1980;22(2):139–145. [PubMed] [Google Scholar]
  95. Waldenström J. G. The benign monoclonal gammapathies: a study of monoclonal antibodies. Ergeb Inn Med Kinderheilkd. 1982;50:31–77. doi: 10.1007/978-3-642-68546-0_2. [DOI] [PubMed] [Google Scholar]
  96. Warner T. F., Krueger R. G. Circulating lymphocytes and the spread of myeloma. Review of the evidence. Lancet. 1978 Jun 3;1(8075):1174–1176. doi: 10.1016/s0140-6736(78)90966-2. [DOI] [PubMed] [Google Scholar]
  97. Warnke R. A., Kim H., Fuks Z., Dorfman R. F. The coexistence of nodular and diffuse patterns in nodular non-Hodgkin's lymphomas: significance and clinicopathologic correlation. Cancer. 1977 Sep;40(3):1229–1233. doi: 10.1002/1097-0142(197709)40:3<1229::aid-cncr2820400337>3.0.co;2-f. [DOI] [PubMed] [Google Scholar]
  98. Woda B. A., Knowles D. M., 2nd Nodular lymphocytic lymphoma eventuating into diffuse histiocytic lymphoma: immunoperoxidase demonstration of monoclonality. Cancer. 1979 Jan;43(1):303–307. doi: 10.1002/1097-0142(197901)43:1<303::aid-cncr2820430144>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
  99. Wright D. H. The identification and classification of non-hodgkin's lymphoma: A review. Diagn Histopathol. 1982 Apr-Jun;5(2):73–111. [PubMed] [Google Scholar]
  100. Wutke K., Várbíró M., Rüdiger K. D., Kelényi G. Cytological and histological classification of multiple myeloma. Haematologia (Budap) 1981;14(3):315–329. [PubMed] [Google Scholar]
  101. Zalcberg J. R., Cornell F. N., Ireton H. J., McGrath K. M., McLachlan R., Woodruff R. K., Wiley J. S. Chronic lymphatic leukemia developing in a patient with multiple myeloma: immunologic demonstration of a clonally distinct second malignancy. Cancer. 1982 Aug 1;50(3):594–597. doi: 10.1002/1097-0142(19820801)50:3<594::aid-cncr2820500335>3.0.co;2-e. [DOI] [PubMed] [Google Scholar]
  102. Zucker-Franklin D., Amorosi E. L., Ritz N. D. Evolution of Sézary syndrome in the course of hairy cell leukemia. Blood. 1982 Jun;59(6):1181–1190. [PubMed] [Google Scholar]

Articles from Journal of Clinical Pathology are provided here courtesy of BMJ Publishing Group

RESOURCES