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Molecular Diagnosis & Therapy

, Volume 11, Issue 1, pp 29–53 | Cite as

Diagnostic Impact of Molecular Lineage Analysis on Paraffin-Embedded Tissue in Hematolymphoid Neoplasia Reclassified by Current WHO Criteria

  • Leonard Hwan Cheong Tan
  • Lily-Lily Chiu
  • Evelyn Siew Chuan Koay
Original Research Article

Abstract

Background and Objective: By current WHO criteria, most — though not all — cases of hematolymphoid neoplasm can be diagnosed immunomorphologically, diminishing the role of molecular tests for lymphoid antigen receptor clonality in lymphoma diagnosis. Hence, our objective was to glean immunomorphological and molecular correlates from hematolymphoid neoplasms that had remained unresolvable without diagnostic molecular input.

Methods: Thirty-five such cases were reviewed histologically and with standard immunoperoxidases. In situ hybridization for Epstein-Barr virus (EBV)-encoded RNAs (EBER) was performed on selected cases. PCR amplification of genes encoding T-cell receptors (TcR) and immunoglobulin heavy chains (IgH) [TR and IGH genes, respectively] was performed on whole tissue in all cases, and on microdissected cells in two cases.

Results: Twenty-five cases (71%) requiring diagnostic molecular genotyping had some form of peripheral T-cell lymphoma (PTCL). Twenty (80%) of these were complicated by a proliferation of B-lineage cells, either within the same tissue (‘syntopic’) as large B cells (LBC) or Reed-Sternberg (RS)-like cells (17 cases), florid lymphoid hyperplasia (two cases, one also with syntopic LBC) or monotypic plasma cells (one case), or at a separate (‘metatopic’) site as a B-cell lymphoma (two cases, one of which also had syntopic LBC) or Hodgkin lymphoma (HL; one case, also showing syntopic LBC). Fifteen (75%) of these 20 PTCLs with B-lineage proliferation yielded monoclonal TR gene rearrangements, and only two (10%) showed IGH monoclonality, which was transient in one case. Three (18%) of the PTCLs with LBC had originally been misinterpreted as some form of HL. Conversely, of the remaining cases, three of four (75%) that had been diagnosed initially as some form of large cell non-HL (NHL), including two of three that were called ‘anaplastic’, had to be revised to grade II/syncytial nodular sclerosing (NS) HL, yielding polyclonal TcRγ gene (TRG) rearrangements, with one case, in addition, disclosing a biallelic clonal IGH gene rearrangement that excluded anaplastic large cell lymphoma.

Discussion/Conclusion: Paradoxically, monoclonality of TR rather than IGH gene rearrangement may more often be detectable in a predominantly dispersed (‘hodgkinoid’), large B-lineage cell proliferation, consistent with release from immune regulation in the milieu of impaired immunosurveillance within a PTCL. This is compounded by the difficulty in ascertaining clonal IGH gene rearrangements resulting from (1) poor consensus primer hybridization due to somatic hypermutations, and (2) ‘dilution’ in a T-cell-rich milieu. These same difficulties also account for the long-elusive identification of the RS cell lineage. Conversely, anaplastic lymphoma, which is of non-B lineage, may be mimicked by NSHL, which is of B lineage.

Keywords

Primary Biliary Cirrhosis Anaplastic Lymphoma Kinase Anaplastic Large Cell Lymphoma Classical Hodgkin Lymphoma Nodular Sclerosing Hodgkin Lymphoma 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Dr Puay-Hoon Tan (Singapore General Hospital [SGH]) for her contributions of Cases 5 and 6 as consultations; Dr Danilo Giron (Tan Tock Seng Hospital, Singapore) for contributing Case 10; Dr Amy Chadburn and Dr Elizabeth Hyjek (Weill-Cornell Medical College, New York-Presbyterian Hospital, New York, NY, USA) for sharing Case 14; Dr Norman Chan (Tawam Hospital, Al Ain, Abu Dhabi, UAE) for contributing Case 23; Hui-Qin Lim and Shoa-Nian Choo (National University of Singapore [NUS]), as well as Jane Tan, Maryam Hazly Hilmy and Mei-Jiuan Chng (SGH) for performing the immunohistochemical stains; Adrian Lee (SGH) for performing the molecular work on cases in SGH; Tee-Chok Tan (NUS) for assistance in photomicrography; Jean Chen (National University Hospital [NUH]) for the karyotyping of Case 25; and Wendy Ang (NUH) for configuring the tables in this article.

This work was partly funded by a grant from the Health Services Development Program of the Ministry of Health, Singapore, and partly funded by a grant (no. DCR/P30/06) from the Department of Clinical Research, SGH. The authors have no conflicts of interest that are directly relevant to the content of this study.

Supplementary material

40291_2012_BF03256221_MOESM1_ESM.pdf (154 kb)
Supplementary material, approximately 157 KB.

References

  1. 1.
    Jaffe ES, Harris NL, Stein H, et al. Pathology and genetics: tumors of haematopoeitic and lymphoid tissues. World Health Organization classification of tumours. Lyon: International Agency for Research on Cancer, 2001Google Scholar
  2. 2.
    Gulley ML. Antigen receptor gene rearrangements. In: Leonard DGB, editor. Diagnostic molecular pathology: major problems in pathology. Vol. 41. Philadelphia (PA): Saunders, 2003: 118–24Google Scholar
  3. 3.
    Pan L, Cesarman E, Knowles DM. Antigen receptor genes: structure, function and genetic analysis of their rearrangements. In: Knowles DM, editor. Neoplastic hematopathology. Philadelphia (PA): Williams and Wilkins, 2001: 307–28Google Scholar
  4. 4.
    Antigen receptor genes and analysis of their rearrangements. In: Warnke RA, Weiss LM, Chan JKC, et al., editors. Tumors of the lymph nodes and spleen: atlas of tumor pathology, 3rd series, fascicle 14. Washington DC: US Armed Forces Institute of Pathology, 1994: 31–4Google Scholar
  5. 5.
    Evens AM, Gartenhaus RB. Treatment of T-cell non-Hodgkin’s lymphoma. Curr Treat Options Oncol 2004 Aug; 5(4): 289–303PubMedCrossRefGoogle Scholar
  6. 6.
    Gallamini A, Stelitano C, Calvi R, et al. Peripheral T-cell lymphoma unspecified (PTCL-U): a new prognostic model from a retrospective multicentric clinical study. Blood 2004 Apr; 103(7): 2474–9PubMedCrossRefGoogle Scholar
  7. 7.
    Savage KJ, Chhanabhai M, Gascoyne RD, et al. Characterization of peripheral T-cell lymphomas in a single North American institution by the WHO classification. Ann Oncol 2004 Oct; 15(10): 1467–75PubMedCrossRefGoogle Scholar
  8. 8.
    Sehn LH, Connors JM. Treatment of aggressive non-Hodgkin’s lymphoma: a north American perspective. Oncology (Williston Park) 2005 Apr; 19(4 Suppl. 1): 26–34Google Scholar
  9. 9.
    Coiffier B, Reyes F. Groupe d’Etude des Lymphomes de l’Adulte. Best treatment of aggressive non-Hodgkin’s lymphoma: a French perspective. Oncology (Williston Park) 2005 Apr; 19(4 Suppl. 1): 7–15Google Scholar
  10. 10.
    Fisher RI, Miller TP, O’Connor OA. Diffuse aggressive lymphoma. Hematology (Am Soc Hematol Educ Program) 2004; 2004: 221–36CrossRefGoogle Scholar
  11. 11.
    Younes A. New treatment strategies for aggressive lymphoma. Semin Oncol 2004 Dec; 31(6 Suppl. 15): 10–3PubMedCrossRefGoogle Scholar
  12. 12.
    Coiffier B. Effective immunochemotherapy for aggressive non-Hodgkin’s lymphoma. Semin Oncol 2004 Feb; 31(1 Suppl. 2): 7–11PubMedCrossRefGoogle Scholar
  13. 13.
    Kadin ME. Hodgkin’’s disease: cell of origin, immunobiology and pathogenesis. In: Knowles DM, editor. Neoplastic hematopathology. Philadelphia (PA): Williams and Wilkins, 2001: 667–90Google Scholar
  14. 14.
    Hertel CB, Zhou XG, Hamilton-Dutoit SJ, et al. Loss of B cell identity correlates with loss of B cell-specific transcription factors in Hodgkin/Reed-Sternberg cells of classical Hodgkin lymphoma. Oncogene 2000; 21: 4908–20CrossRefGoogle Scholar
  15. 15.
    Marafioti T, Hummel M, Foss HD, et al. Hodgkin and Reed-Sternberg cells represent an expansion of a single clone originating from a germinal center B-cell with functional immunoglobulin gene rearrangements but defective immunoglobulin transcription. Blood 2000; 95: 1443–50PubMedGoogle Scholar
  16. 16.
    Theil J, Laumen H, Marafioti T, et al. Defective octamer-dependent transcription is responsible for silenced immunoglobulin transcription in Reed-Sternberg cells. Blood 2001 May 15; 97(10): 3191–6PubMedCrossRefGoogle Scholar
  17. 17.
    Harris NL, Jaffe ES, Stein H, et al. A revised European-American classification of lymphoid neoplasms: a proposal from the international lymphoma study group. Blood 1994; 84(5): 1361–92PubMedGoogle Scholar
  18. 18.
    Jaffe ES. Anaplastic large cell lymphoma: the shifting sands of diagnostic hematopathology. Mod Pathol 2001; 14(3): 219–28PubMedCrossRefGoogle Scholar
  19. 19.
    Weisenburger DD, Anderson JR, Diebold J, et al. Systemic anaplastic large-cell lymphoma: results from the non-Hodgkin’s lymphoma classification project. Am J Hematol 2001; 67(3): 172–8PubMedCrossRefGoogle Scholar
  20. 20.
    Tan LHC, Chong SM. Grade II nodular sclerosing Hodgkin lymphoma commonly mimics non-Hodgkin lymphomas with anaplastic morphology: a pathologic review of 42 cases reclassified by current WHO criteria [abstract]. Mod Pathol 2003 Jan; 16(1): 255AGoogle Scholar
  21. 21.
    Tan LHC, Do E, Tan SY, et al. Multi-lineage interrogation of the performance characteristics of a split-signal fluorescence in situ hybridization probe (FISH) for Anaplastic Lymphoma Kinase gene rearrangement: a study of 101 cases characterized by immunohistomorphology on fixed archival tissue. Mol Diagn 2004; 8(4): 213–29PubMedCrossRefGoogle Scholar
  22. 22.
    Tan LHC, Do E, Chong SM, et al. Detection of ALK gene rearrangements in formalin-fixed, paraffin-embedded tissue using a fluorescence in-situ hybridization (FISH) probe: a search for optimum conditions of tissue archiving and preparation for FISH. Mol Diagn 2003 Mar; 7(1): 27–33PubMedCrossRefGoogle Scholar
  23. 23.
    Chang TL, Salto-Tellez M, Thamboo TP, et al. Diagnostic validation of capillary electrophoresis analysis of T-cell receptor γ-chain gene rearrangements: prediction of malignant transformation of cutaneous T-cell lymphoproliferative disorders. Clin Chemistry 2003; 49(3): 513–5CrossRefGoogle Scholar
  24. 24.
    Sioutos N, Bagg A, Michaud GY, et al. Polymerase chain reaction versus Southern blot hybridization: detection of immunoglobulin heavy-chain gene rearrangements. Diagn Mol Pathol 1995 Mar; 4(1): 8–13PubMedCrossRefGoogle Scholar
  25. 25.
    McCarthy KP, Sloane JP, Kabarowski JHS, et al. The rapid detection of clonal T-cell proliferation in patients with lymphoid disorders. Am J Pathol 1991 Apr; 138(4): 821–8PubMedGoogle Scholar
  26. 26.
    Classic Hodgkin’s disease. In: Warnke RA, Weiss LM, Chan JKC, et al., editors. Tumors of the lymph nodes and spleen: atlas of tumor pathology, 3rd series, fascicle 14. Washington DC: US Armed Forces Institute of Pathology, 1994: 227–314Google Scholar
  27. 27.
    Achten R, Verhoef G, Vanuytsel L, et al. Histiocyte-rich, T-cell-rich B-cell lymphoma: a distinct diffuse large B-cell lymphoma subtype showing characteristic morphologic and immunophenotypic features. Histopathology 2002 Jan; 40(1): 31–45PubMedCrossRefGoogle Scholar
  28. 28.
    Achten R, Verhoef G, Vanuytsel L, et al. T-cell/histiocyte-rich large B-cell lymphoma: a distinct clinicopathologic entity. J Clin Oncol 2002 Mar 1; 20(5): 1269–77PubMedCrossRefGoogle Scholar
  29. 29.
    Lim MS, Beaty M, Sorbara L, et al. T-cell/histiocyte-rich large B-cell lymphoma: a heterogeneous entity with derivation from germinal center B cells. Am J Surg Pathol 2002 Nov; 26(11): 1458–66PubMedCrossRefGoogle Scholar
  30. 30.
    Ramsay AD, Smith WJ, Isaacson PG. T-cell-rich B-cell lymphoma. Am J Surg Pathol 1988 Jun; 12(6): 433–43PubMedCrossRefGoogle Scholar
  31. 31.
    Lorenzen J, Li G, Zhao-Hohn M, et al. Angioimmunoblastic lymphadenopathy type of T-cell lymphoma and angioimmunoblastic lymphadenopathy: a clinicopathological and molecular biological study of 13 Chinese patients using polymerase chain reaction and paraffin-embedded tissues. Virchows Arch 1994; 424(6): 593–600PubMedCrossRefGoogle Scholar
  32. 32.
    Jones D, Jorgensen JL, Shahsafaei A, et al. Characteristic proliferations of reticular and dendritic cells in angioimmunoblastic lymphoma. Am J Surg Pathol 1998 Aug; 22(8): 956–64PubMedCrossRefGoogle Scholar
  33. 33.
    Lee S-S, Rudiger T, Odenwald T, et al. Angioimmunoblastic T-cell lymphoma is derived from mature T-helper cells with varying expression and loss of detectable CD4. Int J Cancer 2003; 103: 12–20PubMedCrossRefGoogle Scholar
  34. 34.
    Attygalle A, Al-Jehani R, Diss TC, et al. Neoplastic T cells in angioimmunoblastic T-cell lymphoma express CD10. Blood 2002; 99(2): 627–33PubMedCrossRefGoogle Scholar
  35. 35.
    Kojima M, Nakamura S, Itoh H, et al. Angioimmunoblastic T-cell lymphoma with hyperplastic germinal centers: a clinicopathological and immunohistochemical study of 10 cases. APMIS 2001; 109: 699–706PubMedCrossRefGoogle Scholar
  36. 36.
    Steinhoff M, Hummel M, Assaf C, et al. Cutaneous T cell lymphoma and classic Hodgkin lymphoma of B cell type within a single lymph node: composite lymphoma. J Clin Pathol 2004 Mar; 57(3): 329–31PubMedCrossRefGoogle Scholar
  37. 37.
    Quintanilla-Martinez L, Fend F, Moguel LR, et al. Peripheral T-cell lymphoma with Reed-Sternberg-like cells of B-cell phenotype and genotype associated with Epstein-Barr virus infection. Am J Surg Pathol 1999; 23(10): 1233–40PubMedCrossRefGoogle Scholar
  38. 38.
    Higgins JP, van de Rijn M, Jones CD, et al. Peripheral T-cell lymphoma complicated by a proliferation of large B cells. Am J Clin Pathol 2000; 114(2): 236–47PubMedCrossRefGoogle Scholar
  39. 39.
    Schwarting R, Gerdes J, Durkop H, et al. Ber-H2: a new anti-Ki-1 (CD30) monoclonal antibody directed at a formol-resistant epitope. Blood 1989 Oct; 74(5): 1678–89PubMedGoogle Scholar
  40. 40.
    Piris M, Brown DC, Gatter KC, et al. CD30 expression in non-Hodgkin’s lymphoma. Histopathology 1990 Sep; 17(3): 211–8PubMedCrossRefGoogle Scholar
  41. 41.
    Lukes RL, Tindle BH. Immunoblastic lymphadenopathy: a hyperimmune entity resembling Hodgkin’s disease. N Engl J Med 1975 Jan 2; 292(1): 1–8PubMedCrossRefGoogle Scholar
  42. 42.
    Knecht H, Berger C, Rothenberger S, et al. The role of Epstein-Barr virus in neoplastic transformation. Oncology 2001; 60: 289–302PubMedCrossRefGoogle Scholar
  43. 43.
    Lome-Maldonado C, Canioni D, Hermine O, et al. Angio-immunoblastic T cell lymphoma (AILD-TL) rich in large B cells and associated with Epstein-Barr virus infection: a different subtype of AILD-TL? Leukemia 2002; 16: 2134–41PubMedCrossRefGoogle Scholar
  44. 44.
    Zettl A, Lee SS, Rudiger T, et al. Epstein-Barr virus-associated B-cell lymphoproliferative disorders in angioimmunoblastic T-cell lymphoma and peripheral T-cell lymphoma, unspecified. Am J Clin Pathol 2002; 117(3): 368–79PubMedCrossRefGoogle Scholar
  45. 45.
    Ho JWY, Ho FSC, Chan ACL, et al. Frequent detection of Epstein-Barr virus-infected B cells in peripheral T-cell lymphomas. J Pathol 1998; 185: 79–85PubMedCrossRefGoogle Scholar
  46. 46.
    Nakamura S, Sasajima Y, Koshikawa T, et al. Angioimmunoblastic T-cell lymphoma (angioimmunoblastic lymphadenopathy with dysproteinemia [AILD]-type T-cell lymphoma) followed by Hodgkin’s disease associated with Epstein-Barr virus. Pathol Int 1995; 45(120): 958–64PubMedCrossRefGoogle Scholar
  47. 47.
    Willenbrock K, Roes A, Seidl C, et al. 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-β gene rearrangements. Am J Pathol 2001; 158(5): 1851–7PubMedCrossRefGoogle Scholar
  48. 48.
    Smith JL, Hodges E, Quin CT, et al. Frequent T and B cell oligoclones in histologically and immunophenotypically characterized angioimmunoblastic lymphadenopathy. Am J Pathol 2000 Feb; 156(2): 661–9PubMedCrossRefGoogle Scholar
  49. 49.
    Diss TC, Watts M, Pan LX, et al. The polymerase chain reaction in the detection of monoclonality in T-cell lymphomas. J Clin Pathol 1995; 48: 1045–50PubMedCrossRefGoogle Scholar
  50. 50.
    Polliack A, Lugassy G. Autoimmunity and auto-immune syndromes associated with and preceding the development of lymphoproliferative disorders. Leukemia 1992; 6Suppl. 4: 152–4PubMedGoogle Scholar
  51. 51.
    Pavlidis NA, Klouvas G, Tsokos M, et al. Cutaneous lymphocytic vasculopathy in lymphoproliferative disorders: a paraneoplastic lymphocytic vasculitis of the skin. Leuk Lymphoma 1995; 16(5-6): 477–82PubMedCrossRefGoogle Scholar
  52. 52.
    Yataganas X, Papadimitriou C, Pangalis G, et al. Angio-immunoblastic lymphadenopathy terminating as Hodgkin’s disease. Cancer 1977 May; 39(5): 2183–9PubMedCrossRefGoogle Scholar
  53. 53.
    Diss TC, Peng H, Wotherspoon AC, et al. Detection of monoclonality in low-grade B-cell lymphomas using the polymerase chain reaction is dependent on primer selection and lymphoma type. J Pathol 1993 Mar; 169(3): 291–5PubMedCrossRefGoogle Scholar
  54. 54.
    Nakamura N, Kuze T, Hashimoto Y, et al. Analysis of the immunoglobulin heavy chain gene variable region of 101 cases with peripheral B cell neoplasms and B cell chronic lymphocytic leukemia in the Japanese population. Pathol Int 1999 Jul; 49(7): 595–600PubMedCrossRefGoogle Scholar
  55. 55.
    Stein H, Foss HD, Durkop H, et al. CD30+ anaplastic large cell lymphoma: a review of its histopathologic, genetic, and clinical features. Blood 2000 Dec 1; 96(12): 3681–95PubMedGoogle Scholar
  56. 56.
    Foss HD, Reusch R, Demel G, et al. Frequent expression of the B-cell-specific activator protein in Reed-Sternberg cells of classical Hodgkin’s disease provides further evidence for its B-cell origin. Blood 1999 Nov 1; 94(9): 3108–13PubMedGoogle Scholar
  57. 57.
    Delsol G, Lamant L, Mariame B, et al. A new subtype of large B-cell lymphoma expressing the ALK kinase and lacking the 2; 5 translocation. Blood 1997 Mar 1; 89(5): 1483–90PubMedGoogle Scholar
  58. 58.
    Gascoyne RD, Lamant L, Martin-Suberto JI, et al. ALK-positive diffuse large B-cell lymphoma is associated with Clathrin-ALK rearrangements: report of 6 cases. Blood 2003 Oct; 102(7): 2568–73PubMedCrossRefGoogle Scholar
  59. 59.
    De Paepe P, Baens M, van Krieken H, et al. ALK activation by the CLTC-ALK fusion is a recurrent event in large B-cell lymphoma. Blood 2003 Oct; 102(7): 2638–41PubMedCrossRefGoogle Scholar
  60. 60.
    Onciu M, Behm FG, Downing JR, et al. ALK-positive plasmablastic B-cell lymphoma with expression of the NPM-ALK fusion transcript: report of 2 cases. Blood 2003 Oct; 102(7): 2642–4PubMedCrossRefGoogle Scholar
  61. 61.
    Falini B, Pulford K, Pucciarini A, et al. Lymphomas expressing ALK fusion protein(s) other than NPM-ALK. Blood 1999 Nov 15; 94(10): 3509–15PubMedGoogle Scholar
  62. 62.
    Pulford K, Lamant L, Morris SW, et al. Detection of anaplastic lymphoma kinase (ALK) and nucleolar protein nucleophosmin (NPM)-ALK proteins in normal and neoplastic cells with the monoclonal antibody ALK1. Blood 1997 Feb; 89(4): 1394–404PubMedGoogle Scholar
  63. 63.
    Tan LHC. ALK-positive anaplastic T-cell lymphoma, combined small-cell/ lymphohistiocytic variant, mimicking Kikuchi-Fujimoto (subacute/histiocytic necrotizing) lymphadenitis. In: Cooke RA, editor. Surgical pathology: a Singapore-Malaysia experience. Slide seminar, XXV Congress of the International Academy of Pathology; 2004 Oct 11–16; Brisbane. Brisbane: Knowledge Books and Software, 2004: 79–89Google Scholar
  64. 64.
    Beaubier NT, Hart AP, Bartolo C, et al. Comparison of capillary electrophoresis and polyacrylamide gel electrophoresis for the evaluation of T and B cell clonality by polymerase chain reaction. Diagn Mol Pathol 2000; 9(3): 121–31PubMedCrossRefGoogle Scholar
  65. 65.
    Sprouse J, Werling R, Hanke D, et al. T-cell clonality determination using polymerase chain reaction (PCR) amplification of the T-cell receptor gammachain gene and capillary electrophoresis of fluorescently-labelled products. Am J Clin Pathol 2000; 113: 838–50PubMedCrossRefGoogle Scholar
  66. 66.
    Simon M, Kind P, Kaudewitz P, et al. Automated high-resolution polymerase chain reaction fragment analysis. A method for detecting T-cell receptor gammachain gene rearrangements in lymphoproliferative diseases. Am J Pathol 1998; 152(1): 29–33PubMedGoogle Scholar
  67. 67.
    Benharroch D, Meguerian-Bedoyan Z, Lamant L, et al. ALK-positive lymphoma: a single disease with a broad spectrum of morphology. Blood 1998 Mar 15; 91(6): 2076–84PubMedGoogle Scholar
  68. 68.
    Tan LHC, Chen CS, Mow BMF, et al. Medullary myeloid disorders in young patients negate large-cell lymphoma and favor extramedullary myeloblastic tumor/granulocytic sarcoma. Proceedings of the 4th Asia-Pacific International Academy of Pathology Congress; 2005 Aug 23–26; Beijing. Bologna: Medimond International Proceedings, 2005: 119–23Google Scholar
  69. 69.
    Sanchez I, San Miguel JF, Corral J, et al. Gene rearrangement in acute non-lymphoblastic leukaemia: correlation with morphological and immunophenotypic characteristics of blast cells. Br J Haematol 1995 Jan; 89(1): 104–9PubMedCrossRefGoogle Scholar
  70. 70.
    Paietta E, Van Ness B, Bennett J, et al. Lymphoid lineage-associated features in acute myeloid leukaemia: phenotypic and genotypic correlations. Br J Haematol 1992 Oct; 82(2): 324–31PubMedCrossRefGoogle Scholar
  71. 71.
    Rudiger T, Jaffe ES, Delsol G, et al. Workshop report on Hodgkin’s disease and related diseases (‘grey zone’ lymphoma). Ann Oncol 1998; 9Suppl. 5: S31–8PubMedCrossRefGoogle Scholar
  72. 72.
    Mohrmann RL, Arber DA. CD20-positive peripheral T-cell lymphoma: report of a case after nodular sclerosis Hodgkin’ s disease and review of the literature. Mod Pathol 2000 Nov; 13(11): 1244–52PubMedCrossRefGoogle Scholar
  73. 73.
    Hodges E, Krishna MT, Pickard C, et al. Diagnostic role of tests for T cell receptor (TCR) genes. J Clin Pathol 2003; 56: 1–11PubMedCrossRefGoogle Scholar
  74. 74.
    Ye MQ, Suriawinata A, Black C, et al. Primary hepatic marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue type in a patient with primary biliary cirrhosis. Arch Pathol Lab Med 2000 Apr; 124(4): 604–8PubMedGoogle Scholar
  75. 75.
    Prabhu RM, Medeiros LJ, Kumar D, et al. Primary hepatic low-grade B-cell lymphoma of mucosa-associated lymphoid tissue (MALT) associated with primary biliary cirrhosis. Mod Pathol 1998 Apr; 11(4): 404–10PubMedGoogle Scholar
  76. 76.
    Stroehmann A, Dorner T, Lukowsky A, et al. Cutaneous T cell lymphoma in a patient with primary biliary cirrhosis and secondary Sjogren’s syndrome. J Rheumatol 2002 Jun; 29(6): 1326–9PubMedGoogle Scholar
  77. 77.
    Childs CC, Parham DM, Berard CW. Infectious mononucleosis. The spectrum of morphologic changes simulating lymphoma in lymph nodes and tonsils. Am J Surg Pathol 1987 Feb; 11(2): 122–32PubMedCrossRefGoogle Scholar
  78. 78.
    Tindle BH, Parker JW, Lukes RJ. “Reed-Sternberg cells” in infectious mononucleosis? Am J Clin Pathol 1972 Dec; 58(6): 607–17PubMedGoogle Scholar
  79. 79.
    Lukes RJ. Criteria for involvement of lymph node, bone marrow, spleen, and liver in Hodgkin’s disease. Cancer Res 1971 Nov; 31(11): 1755–67PubMedGoogle Scholar
  80. 80.
    Kadin ME, Glatstein E, Dorfman RF. Clinicopathologic studies of 117 untreated patients subjected to laparotomy for the staging of Hodgkin’s disease. Cancer 1971 Jun; 27(6): 1277–94PubMedCrossRefGoogle Scholar
  81. 81.
    Van Parys G, de Wolf-Peeters C, van den Oord JJ, et al. Lymph node architecture in Hodgkin’s disease: evidence for the role of the composite nodule in nodular sclerosing Hodgkin’s disease. Hematol Oncol 1987 Apr–Jun; 5(2): 147–54PubMedCrossRefGoogle Scholar
  82. 82.
    Anagnostopoulos I, Hansmann ML, Franssila K, et al. European Task Force on Lymphoma project on lymphocyte predominance Hodgkin disease: histologic and immunohistologic analysis of submitted cases reveals 2 types of Hodgkin disease with a nodular growth pattern and abundant lymphocytes. Blood 2000 Sep 1; 96(5): 1889–99PubMedGoogle Scholar
  83. 83.
    Cabone A, Gloghini A, Gaidano G, et al. Expression status of BCL-6 and syndecan-1 identifies distinct histogenetic subtypes of Hodgkin’s disease. Blood 1998 Oct 1; 92(7): 2220–8Google Scholar
  84. 84.
    Carbone A, Gloghini A, Aldinucci D, et al. Expression pattern of MUM1/IRF4 in the spectrum of pathology of Hodgkin’s disease. Br J Haematol 2002 May; 117(2): 366–72PubMedCrossRefGoogle Scholar
  85. 85.
    Skinnider BF, Mak TW. The role of cytokines in classical Hodgkin lymphoma. Blood 2002 Jun 15; 99(12): 4283–97PubMedCrossRefGoogle Scholar
  86. 86.
    Tsang WY, Chan JK, Sing C. The nature of Reed-Sternberg-like cells in chronic lymphocytic leukemia. Am J Clin Pathol 1993 Mar; 99(3): 317–23PubMedGoogle Scholar
  87. 87.
    Roers A, Montesinos-Rongen M, Hansmann ML, et al. Amplification of TCRbeta gene rearrangements from micromanipulated single cells: T cells rosetting around Hodgkin and Reed-Sternberg cells in Hodgkin’s disease are polyclonal. Eur J Immunol 1998 Aug; 28(8): 2424–31PubMedCrossRefGoogle Scholar
  88. 88.
    Poppema S, Potters M, Visser L, et al. Immune escape mechanisms in Hodgkin’s disease. Ann Oncol 1998; 9Suppl. 5: S21–4PubMedCrossRefGoogle Scholar
  89. 89.
    Cazals-Hatem D, Andre M, Mounier N, et al. Pathologic and clinical features of 77 Hodgkin’s lymphoma patients treated in a lymphoma protocol (LNH87). Am J Surg Pathol 2001 Mar; 25(3): 297–306PubMedCrossRefGoogle Scholar
  90. 90.
    Brousset P, Rochaix P, Chittal S, et al. High incidence of Epstein-Barr virus detection in Hodgkin’s disease and absence of detection in anaplastic large-cell lymphoma in children. Histopathology 1993 Aug; 23(2): 189–91PubMedCrossRefGoogle Scholar
  91. 91.
    Calame C, Lin K-I, Tunyaplin C. Regulatory mechanisms that determine the development and function of plasma cells. Annu Rev Immunol 2003; 21: 205–30PubMedCrossRefGoogle Scholar
  92. 92.
    Dong HY, Scadden DT, de Levai L, et al. Plasmablastic lymphoma in HIV-positive patients: an aggressive Epstein-Barr virus-associated extramedullary plasmacytic neoplasm. Am J Surg Pathol 2005 Dec; 29(12): 1633–41PubMedCrossRefGoogle Scholar
  93. 93.
    Vega F, Chang CC, Medeiros LJ, et al. Plasmablastic lymphomas and plasmablastic plasma cell myelomas have nearly identical immunophenotypic profiles. Mod Pathol 2005 Jun; 18(6): 806–15PubMedCrossRefGoogle Scholar
  94. 94.
    Colomo L, Loong F, Rives S, et al. Diffuse large B-cell lymphomas with plasmablastic differentiation represent a heterogeneous group of disease entities. Am J Surg Pathol 2004 Jun; 28(6): 736–47PubMedCrossRefGoogle Scholar
  95. 95.
    Dawson-Saunders B, Trapp RG. Basic and clinical biostatistics. London: Prentice-Hall, 1994: 143–61Google Scholar
  96. 96.
    Seow A, Koh WP, Chia KS, et al. Trends in cancer incidence in Singapore 1968-2002. Report No. 6. Singapore: Singapore Cancer Registry, 2004Google Scholar

Copyright information

© Adis Data Information BV 2007

Authors and Affiliations

  • Leonard Hwan Cheong Tan
    • 1
    • 2
  • Lily-Lily Chiu
    • 3
  • Evelyn Siew Chuan Koay
    • 1
    • 3
  1. 1.Department of Pathology, Yong Loo Lin School of MedicineNational University of SingaporeSingapore
  2. 2.Department of PathologySingapore General HospitalSingapore
  3. 3.Molecular Diagnosis Centre, Department of Laboratory MedicineNational University HospitalSingapore

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