Canine T-cell Lymphomas: A Morphological, Immunological, and Clinical Study of 46 New Cases

Veterinary Pathology

Volumn 39, Issue 1, 2002, Pages 92-109

  Fournel Fleury, C ^a   Ponce, F ^a   Felman, P ^b   Blavier, A ^a   Bonnefont, C ^a   Chabanne, L ^a   Marchal, T ^a   Cadore, J L ^a   Goy Thollot, I ^a   Ledieu, D ^a   Ghernati, I ^a   Magnol, J P ^a  

^a VETAGRO SUP   (France)

^b CENTRE HOSPITALIER LYON SUD   (France)

Author keywords

Canine; classification; immunophenotyping; malignant lymphoma; T cell lymphoma

Indexed keywords

ANIMAL; ANIMAL DISEASE; ARTICLE; BIOPSY; DIFFERENTIAL DIAGNOSIS; DOG; DOG DISEASE; FRANCE; IMMUNOLOGY; IMMUNOPHENOTYPING; INCIDENCE; METHODOLOGY; NEEDLE BIOPSY; PATHOLOGY; T CELL LYMPHOMA;

ANIMALS; BIOPSY; BIOPSY, NEEDLE; DIAGNOSIS, DIFFERENTIAL; DOG DISEASES; DOGS; FRANCE; IMMUNOPHENOTYPING; INCIDENCE; LYMPHOMA, T-CELL;

EID: 18744371285     PISSN: 03009858     EISSN: 15444221     Source Type: Journal    
DOI: 10.1354/vp.39-1-92     Document Type: Article

References (96)

1. Appelbaum FR, Sale GE, Storb R, Charrier K, Deeg HJ, Graham T, Wulff JC: Phenotyping of canine lymphoma with monoclonal antibodies directed against cell surface antigens: classification, morphology, clinical presentation, and response to chemotherapy. Haematol Oncol 2: 151–158, 1984
2. Ascani S, Zinzani PL, Gherlinzoni F, Sabattini E, Briskomatis A, De Vivo A, Piccioli M, Fraternali Orcioni G, Pieri F, Goldoni A, Piccaluga PP, Zallocco D, Burnelli R, Leoncini L, Falini B, Tura S, Pileri SA: Peripheral Tcell lymphomas. Clinico-pathologic study of 168 cases diagnosed according to the R.E.A.L. classification. Annals of Oncol 8: 583–592, 1997
3. Bäckgren AW: Lymphatic leukosis in dogs. An epizootological clinical and haematological study. Acta Vet Scand 6(Suppl 1): 7–80, 1965
4. Ballerini P, Gaidano G, Gong J, Tassi V, Saglio G, Knowles D, Dalla-Favera R: Multiple genetic lesions in AIDS-related non-Hodgkin lymphoma. Blood 81: 166, 1993
5. Bernard A, Boumsell L, Reinherz L, et al.:Cell surface characterization of malignant T-cells from lymphoblastic lymphoma using monoclonal antibodies: evidence for phenotypic differences between malignant T-cells from patients with acute lymphoblastic leukemia and lymphoblastic lymphomas. Blood 57: 1105–1113, 1981
6. Brenner MB, McLean J, Scheft M, Warnke RA, Jones N, Strominger JL: Characterization and expression of the human β-cell receptor using a framework monoclonal antibody. J Immunol 138: 1502–1507, 1987
7. Carter RF, Valli VEO: Advances in the cytologic diagnosis of canine lymphoma. Semin Vet Med surg (Small Anim) 3: 167–175, 1988
8. Carter RF, Valli VEO, Lumsden JH: The cytology, histology and prevalence of cell types in canine lymphoma classified according the National Cancer Institute Working Formulation. Can J Vet Res 50: 154–164, 1986
9. Cartwright R, Brincker H, Carli PM, Clayden D, Coebergh JW, Jack A, McNally R, Morgan G, De Sanjose S, Tumino R, Vornanen M: The rise in incidence of lymphomas in Europe 1985–1992. Eur J Cancer 35: 627–633, 1999
10. Chabanne L, Marchal T, Kaplanski C, Fournel-Fleury C, Magnol JP, Monier JC, Rigal D: Screening of 78 monoclonal antibodies directed against human leukocyte antigens for cross-reactivity with surface markers on canine lymphocytes. Tissue Antigens 43: 202–205, 1994
11. Chadburn A, Knowles DM: Paraffin-resistant antigens detectable by antibodies L26 and polyclonal CD3 predict the B- or T-cell lineage of 95% of diffuse aggressive non Hodgkin's lymphomas. Am J Clin Pathol 102: 284–291, 1994
12. Chassagne-Ckément C, Blay JY, Treilleux I, Sebban C, Bergeron C, Biron P, Philip T: Epidémiologie des lymphomes malins non hodgkiniens: données actualisées. Bull Cancer 86: 529–536, 1999
13. Chew DJ, Meuten DJ: Disorders of calcium and phosphorus metabolism. Vet Clin North Am 12: 411–438, 1982
14. Cobbold SP, Metcalfe S: Monoclonal antibodies that define canine homologues of human CD antigens: summary of the First International Canine Leukocyte AntigenWorkshop (CLAW). Tissue Antigens 43: 137–154, 1994
15. Coiffier B: Lymphomes malin non-Hodgkiniens. Rev Prat Paris 43: 1615–1616, 1993
16. Coiffier B, Berger F, Bryon PA, Magaud JP: T-cell lymphomas: immunologic, histologic, clinical and therapeutic analysis of 63 cases. J Clin Oncol 6: 1584–1591, 1988
17. Coiffier B, Brousse N, Peuchmaur M, Berger F, Gisselbrecht C, Bryon PA, Diebold J for the GELA (Groupe d'Etude des Lymphomes Agressives): Peripheral T-cell lymphomas have a worse prognosis than B-cell lymphomas: a prospective study of 361 immunophenotyped patients treated with the LNH-84 regimen. Annals Oncol 1: 45–50, 1990
18. Day MJ: Immunophenotypic characterization of cutaneous lymphoid neoplasia in the dog and cat. J Comp Pathol 112: 79–96, 1995
19. Delverdier M, Buchet M, van Haverbeke G: Histologie et cytologie des lymphomes malins canins. Etude comparative des classifications actuelles. Rev Med Vet 139: 1141–1150, 1988
20. Felman P, Gentilhomme O: Atlas de Cytopathologie Ganglionnaire. Arnette, Paris, France, 1997
21. Ferrer L, Fondevila D, Rabanal R, Ramis A: Detection of T lymphocytes in canine tissue embedded in paraffin wax by means of antibody to CD3 antigen. J Comp Pathol 106: 311–314, 1992
22. Fisher DJ, Naydan D, Werner LL, Moore PF: Immunophenotyping lymphomas in dogs: a comparison of results from fine needle aspirate and needle biopsy samples. Vet Clin Pathol 24: 118–123, 1995
23. Fournel-Fleury C, Magnol JP, Bricaire P, Marchal T, Chabanne L, Delverdier A, Bryon PA, Felman P: Cytohistological and immunological classification of canine malignant lymphomas. Comparison with human non-Hodgkin's lymphomas. J Comp Pathol 117: 35–39, 1997
24. Fournel-Fleury C, Magnol JP, Chabanne L, Ghernati I, Marchal T, Bonnefont C, Bryon PA, Felman P: Growth fractions in canine non-Hodgkin's lymphomas as determined in situ by the expression of the Ki-67 antigen. J Comp Pathol 117: 61–72, 1997
25. Fournel-Fleury C, Magnol JP, Guelfi JF: Atlas en Couleur de Cytologie du Cancer chez le Chien et le Chat/Color Atlas of Cancer Cytology of the Dog and Cat. Pratique Médicale et Chirurgicale de l'Animal de Compagnie, Paris, France, 1994
26. Ghernati I, Auger C, Chabanne L, Corbin A, Bonnefont C, Magnol JP, Fournel C, Rivoire A, Monier JC, Rigal D: Characterization of a canine long-term T cell line (DLC 01) established from a dog with Sézary syndrome and producing retroviral particles. Leuk 13: 1281–1290, 1999
27. Ghernati I, Corbin A, Chabanne L, Auger C, Magnol JP, Fournel C, Monier JC, Darlix JL, Rigal D: Canine large granular lymphocyte leukemia and its derived cell line produce infectious retroviral particles. Vet Pathol 37: 4, 310–317,2000
28. Greenlee PG, Filippa DA, Quimby F, Patnaik AK, Calvano SE, Matus RE, Kimmel M, Hurvitz AI: Lymphomas in dogs. A morphologic, immunologic and clinical study. Cancer 66: 480–490, 1990
29. Grogan TM, Fielder K, Rangel C, Jolley CJ, Wirt DP, Hicks MJ, Miller TP, Brooks R, Greenberger B, Jones S: Peripheral T-cell lymphomas aggressive disease with heterogeneous immunotypes. Am J Pathol 120: 356–370, 1985
30. Grossman B, Schechter GP, Horton JE, Pierce L, Jaffe E, Whal L: Hypercalcemia associated with T-cell lymphoma-leukemia. Am J Clin Pathol 75: 149–155, 1981
31. Haga T, Yokomori K, Nakayama H, Hayashi T, Goto N, Takahashi R, Fujiwara K: Canine and feline lymphoid and myeloid tumors encountered in Tokyo. Jpn J Vet Sci 50: 809–813, 1988
32. Hamilton-Dutoit S, Pallesen G, Franzmann M, Karkov J, Black F, Skinhoj P, Pedersen C: AIDS-related lymphoma. Histopathology, immunophenotype, and association with Epstein-Barr virus as demonstrated by in situ nucleic acid hybridization. Am J Pathol 138: 149–163, 1991
33. Harabuchi Y, Imai S, Wakashima J, Hirao M, Kataura A, Osato T, Kon S: Nasal T-cell lymphoma casually associated with Epstein-Barr virus. Clinicopathologic, phenotypic and genotypic studies. Cancer 77: 2137–2149, 1996
34. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JKC, Cleary ML, Delsol G, De Woolf-Peeters C, Falini B, Gatter KC, Grogan TM, Isaacson PG, Knowles DM, Mason DY, Mueller-Hermeling HK, Pileri SA, Piris MA, Ralfkiaer E, Warnke RA: A revised European–American classification of lymphoid neoplasms: a proposal from the international study group. Blood 84: 1361–1392, 1994
35. Hayes HM: The comparative epidemiology of selected neoplasms between dogs, cats and humans. A review. Eur J Cancer 14: 1299–1308, 1978
36. Hayes HM, Tarone RE, Cantor KP, Jessen CR, Mac Curnin DM, Richardson RC: Case-control study of canine malignant lymphoma: positive association with dog owner's use of 2,4-dichlorophenoxyacetic acid herbicides. J Natl Cancer Inst 83: 1226–1231, 1991
37. Henni T, Gaulard PH, Divine M, et al.:Comparison of genetic probe with immunophenotypic analysis in lymphoproliferative disorders: a study of 87 cases. Blood 72: 1937–1942, 1988
38. Horning SJ, Weiss LM, Crabtree GS, Warnke RA: Clinical and phenotypic diversity of T-cell lymphomas. Blood 67: 1578–1590, 1986
39. Jaffe ES: Hematopathology: integration of morphologic features and biologic markers for diagnosis. Mod Pathol 12: 109–115, 1999
40. Jaffe ES: Surgical Pathology of the Lymph Nodes and Related Organs, 2nd ed., PA Saunders, Philadelphia, PA, 1995
41. Jaffe E, Blattner W, Blayney D, Bunn P, Cossman J, Robert-Guroff M, Gallo R: The pathologic spectrum of adult T-cell leukemia/lymphoma in the United States. Am J Surg Pathol 8: 263–275, 1984
42. Jaffe ES, Krenacs L, Raffeld M: Classification of T-cell and NK-cell neoplasms based on the REAL classification. Annals of Oncol 8(Suppl 2):S17–S24, 1997
43. Jones M: Peptide Immunisation as a Source of Crossspecies Reactive Antisera Recognizing Leukocyte Differentiation Antigens. Immunological Reagents for the Study of Disease in Companion Animals. The Wellcome Trust, London, UK, 1993
44. Jones M, Cordell JL, Beyers AD, Tse AGD, Mason DY: Detection of T and B cells in many animal species using cross-reactive anti-peptide antibodies. J Immunol 150: 5429–5435, 1993
45. Kariya K, Konno A, Ishida T: Perforin-like immunoreactivity in four cases of lymphoma of large granular lymphocytes in the cat. Vet Pathol 34: 156–159, 1997
46. Khan G, Norton AJ, Slavin G: Epstein-Barr virus in angio-immunoblastic T-cell lymhoma. Histopathology 22: 145–149, 1993
47. Kinoshita K, Kamihira S, Ikeda S, Yamada Y, Muta T, Kitamura T, Ichimaru M, Matsuo T: Clinical, hematologic and pathologic features of leukemic T-cell lymphoma. Cancer 50: 1554–1562, 1982
48. Kiupel M, Teske E, Bostock D: Prognostic factors for treated canine malignant lymphoma. Vet pathol 36: 292–300, 1999
49. Knowles DM: Immunophenotypic and antigen receptor gene rearrangement analysis in T-cell neoplasia. Am J Pathol 134: 761–785, 1989
50. Konno A, Hashimoto Y, Kon Y, Sugimura M: Perforinlike immunoreactivity in feline globule leukocytes and their distribution. J Vet Med Sci 56: 1101–1105, 1994
51. Ladiges WC, Keast M, Appelbaum F, Storb R: Phenotypic characterization of canine lymphoma using monoclonal antibodies and a microlymphocytotoxicity assay. Am J Vet Res 49: 870–872, 1988
52. Lennert K, Feller CA: Histologie des Lymphomes Malins Non Hodgkiniens Selon la Classification de Kiel Actualisée. Doin, Paris, France, 1991
53. Lennert K, Mohri N, Stein H, Kaiserling E, Müller-Hermelink HK: Malignant lymphomas other than Hodgkin's disease. In: Handbuch der Speziellen Pathologischen Anatomie und Histologie, pp. 1–833. Springer, Berlin, Heidelberg, Germany, 1978
54. MacEwen EG: Spontaneous tumors in dogs and cats: Models for the study of cancer biology and treatment. Cancer Metastasis Rev 9: 125–135, 1990
55. MacKenzie JL, Fabre JW: Studies with a monoclonal antibody on the distribution of Thy-1 in the lymphoid and extracellular connective tissues of the dog. Transplantation 31: 275–281, 1981
56. Madewell BR: Hematological and bone marrow cytological abnormalities in 75 dogs with malignant lymphomas. J Am Anim Hosp Assoc 22: 235–240, 1986
57. Magnol JP, Ghernati I, Marchal T, Chabanne L, Delverdier A, Fournel-Fleury C: Données cliniques, morphologiques et immunophénotypiques à partir de 10 observations de lymphome T cutanéo-muqueux épithéliotrope du chien (analogue au mycosis fongoïde). Intérét d'un modèle animal de pathologie spontanée. Bull Acad Natl Med 180: 449–462, 1996
58. Mason DY, Cordell JL, Tse AGD, Van Dongen JJM, Van Noesel CJM, Micklem K, Pulfort KA, Valensi F, Comans-Bitter WM, Borst J, Gatter KC: The IgM-associated protein mb-1 as a marker of normal and neoplastic B cells. J Immunol 147: 2474–2482, 1991
59. McDonough SP, Moore PF: Clinical, hematologic, and immunophenotypic characterization of canine large granular lymphocytosis. Vet pathol 37: 637–646, 2000
60. Moore PF, Olivry T, Naydan D: Canine cutaneous epitheliotropic lymphoma (mycosis fungoides) is a proliferative disorder of CD8+ T cells. Am J Pathol 144: 421–429, 1994
61. Moore PF, Rossito PV, Danilenko DM: Canine leukocyte integrins: characterization of a CD18 homologue. Tissue antigens 36: 211–220, 1990
62. Moore PF, Rossito PV, Danilenko DM, Wielenga JJ, Raff RF, and Severns E: Monoclonal antibodies specific for canine CD4 and CD8 define functional T-lymphocyte subsets and high-density expression of CD4 by canine neutrophils. Tissue Antigens 40: 75–85, 1992
63. Moore PF, Schrenzel MD, Affolter VK, Olivry T, Naydan D: Canine cutaneous histiocytoma is an epidermotropic Langerhans cell histiocytosis that expresses CD1 and specific b2 integrin molecules. Am J Pathol 148: 1699–1708, 1996
64. Morel P, Lepage E, Brice P, Dupriez B, D'Agay MF, Fenaux P, Gosselin B, Bauters F, Gisselbrecht C: Prognosis and treatment of lymphoblastic lymphoma in adults. A report on 80 patients. J Clin Oncol 10: 1078–1085, 1992
65. Morgan G, Vornanen M, Puitinen J, Naukkarinen A, Brincker H, Olsen J, Coeburgh JW, Vrints LW, Clayden D, McNally R, Jack A, Carli PM, Petrella T, Tomino R, D'Lollo S, Barchielli A, Cartwright R: On behalf of the biomed study group. Changing trends in the incidence of non-Hodgkin's lymphoma in Europe. Ann Oncol 8(Suppl 2):S49–S54, 1997
66. Nathwani BN, Diamond LW, Winberg CD, Kim H, Bearman RM, Glick JH, Jones SE, Gams RA, Nissen Ni, Rappaport H: Lymphoblastic lymphoma. A clinicopathologic study of 95 patients. Cancer 48: 2347–2357, 1981
67. National Cancer Institute. The non-Hodgkin's lymphoma pathologic classification project: National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphomas. Summary and description of a working formulation for clinical usage. Cancer 49: 2112–2135, 1982
68. Onions D: RNA-dependent DNA polymerase activity in canine lymphosarcoma. Eur J Cancer 16: 345–350, 1980
69. Owen LN, Bostock DE, Betton GR, Onions DE, Holmes J, Yoxall A, Gorman N: The role of spontaneous canine tumours in the evaluation of the etiology and therapy of human cancer. J Small Anim Pract 16: 155–162, 1975
70. Parodi A, Wyers M, Paris J: Incidence of canine lymphoid leukosis. Age, sex and breed distribution: results of a necropsic survey. Proc 3rd Int Symp Comp Leukemia Res, Paris 1967, pp. 263-267, Bibl Haemat 31. Karger, Basel, Switzerland/New York, NY,1968
71. Parodi AL, Dargent F, Crespeau F: Histological classification of canine malignant lymphomas. J Vet Med A 35: 178–192, 1988
72. van Pelt RW, Connor GH: Clinicopathologic survey of malignant lymphoma in the dog. J Am Vet Med Assoc 152: 976–989, 1968
73. Pierrepoint CG: Possible benefits to veterinary medicine of considering the dog as a model for human cancer. J Small Anim Pract 26: 43–47, 1985
74. Pileri SA, Milani M, Fraternali-Orcioni G, Sabattini E: From the R.E.A.L. classification to the upcoming WHO scheme: a step toward universal categorization of lymphoma entities?. Annals Oncol 9: 607–612, 1998
75. Poiesz B, Ruscetti F, Gazdar A: Detection and isolation of type C retrovirus particles from fresh and cultured lymphcytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 77: 7415–7419, 1980
76. Priester WA: Canine lymphoma: relative risk in the boxer breed. J Natl Cancer Inst 39: 833–845, 1967
77. Priester WA, McKay FW: The occurrence of tumors in domestic animals. Bethseda, Maryland, NC1 Monogr 54: 166, 1980
78. Rappaport H: Tumors of the haematopoietic system. In: Atlas of Tumor Pathology, Section 3, fasc. 8, pp. 442. Armed Forces Inst Pathol, Washington, DC, 1966
79. Salhany KE, Cousar JB, Greer JP, Casey TT, Fields JP, Collins RD: Transformation of cutaneous T-cell lymphoma to large cell lymphoma: a clinicopathologic and immunologic study. Am J Pathol 132: 265–277, 1988
80. Sandusky GE, Horton PJ, Wightman KA: Use of monoclonal antibodies to human lymphocytes to identify lymphocyte subsets in lymph nodes of the rhesus monkey and dog. J med Primatol 15: 441–451, 1986
81. Solal-Celigny Ph, Brousse N, Fermé Ch, Gisselbrecht Ch, Reyes F, Coiffier B: Lymphomes, Lymphomes non Hodgkiniens-Maladie de Hodgkin, 3ème ed. Frison-Roche, Paris, France, 1997
82. Squire RA, Bush M, Melby EC, Neeley LM, Yarbrough B: Clinical and pathologic study of canine lymphoma: clinical staging, cell classification, and therapy. J Natl Cancer Inst 56: 565–574, 1973
83. Strandstrom HV, Bowen JM: Canine leukemia-lymphoma complex: a model for human hematopoietic malignancies. In: Advances in Comparative Leukemic Research, ed. Yohn DS, Blakerslee Jr, pp. 447–450. Elsevier, New York, NY, 1998
84. Teske E: Canine malignant lymphoma: a review and comparison with human non-Hondgkin's lymphomas. Vet Quat 4: 209–219, 1994
85. Teske E, Wisman P, Moore PF, Van Heerde P: Histologic classification and immuno-phenotyping of canine non-Hodgkin's lymphomas: unexpected high frequency of T cell lymphomas with B cell morphology. Exp Haematol 22: 1179–1187, 1994
86. The Non-Hodgkin's Lymphoma Classification Project: A clinical evaluation of the International Lymphoma Study Group classification on non-Hodgkin's lymphoma.Blood 89: 3909–3918, 1997
87. Tokunaga M, Sato F: Non-Hodgkin's lymphomas in a southern prefecture in Japan: an analysis of 715 cases. Cancer 46: 1231–1239, 1980
88. Tomley FM, Armstrong SJ, Mahy BWJ, Owen LN: Reverse transcriptase activity and particles of retroviral density in cultured canine lymphosarcoma supernatants. Br J Cancer 47: 277–284, 1983
89. Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchimo H: Adult T-cell leukemia: clinical and hematologic features of 16 cases. Blood 50: 481, 1977
90. Valli VE: Techniques in veterinary cytopathology. Semin Vet Med Surg (Small Anim). 3: 85–93, 1988
91. Vernau W, Moore PF: An immunophenotypic study of canine leukemias and preliminary assessment of clonality by polymerase chain reaction. Vet Immunol Immunopathol 69(2–4):145–164, 1999
92. Weir EC, Greenlee P, Matus R, Brooks M, Morris C, Insogna K: Hypercalcemia in canine lymphosarcoma is associated with the T-cell subtype and with secretion of a PTH-like factor. J Bone Miner Res 3:S106 [Abstract],1988
93. Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M, Isaacson PG: Regression of primary lowgrade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet ii: 575–577, 1993
94. Yamada Y: Phenotypic and functional analysis of leukemic cells from 16 patients with adult T-cell leukemia/lymphoma. Blood 61: 192–199, 1983
95. Zhou XG, Hamilton-Dutoit SJ, Yan QH, Pallesen G: High frequency of Epstein-Barr virus in Chinese peripheral T-cell lymphoma. Histopathology 24: 115–122, 1994
96. Zucca E, Roggero E, Pileri S: B-cell lymphoma of MALT type: A review with special emphasis on diagnostic and management problems of low-grade gastric tumours. Br J Haematol 100: 3–14, 1998