Summary
The task of the present study was to consequently apply a classification for human lymphomas to respective animal tumors and to check for implications that might arise from such a procedure. One hundred and fifty malignant lymphomas from various species were classified according to the modified Rappaport classification and were compared to 200 malignant lymphomas in human patients. The histological tumor type of the animal lymphomas was subsequently compared with the species in which the tumor developed, with the pattern of tumor growth, and with the etiology and pathogenesis. Finally, as far as available, T- and B-cell classifications were presented. The studies show that a classification for human lymphomas can be applied as well to animal lymphomas, although a few exeptions exist: undifferentiated malignant lymphomas of hemocytoblastic type as seen in lower animals are not recognized in man. Contrarily, well differentiated lymphocytic malignant lymphomas are rarely observed in animals and are essentially not present in lower animals. Angioimmunoblastic lymphadenopathy is not yet identified in animals, and reticulum cell sarcoma type B of the mouse (Dunn's classification) has no good counterpart in man.
Most of the virusinduced lymphomas are of lymphocytic type including Burkitt's tumor while there appears no clearcut predominance of any tumor type in chemical carcinogenesis or in spontaneous lymphomagenesis.
In contrast to man where B-cell lymphomas predominate, the laboratory mouse developes a fair number of T-cell lymphomas. No adequate data are available as to the T- or B-cell nature of lymphomas in other species.
There appears to exist no clear correlation between the histological type of experimental lymphomas and their mode of growth, exept that undifferentiated malignant lymphomas of Burkitt's type and of hemocytoblastic type usually develop in one focus and subsequently metastasize.
Although the case material of the present study is limited, the results show that important information may be gained when a uniform tumor classification is applied. In this sense, it is hoped that the presentation may stimulate similar investigations, and an outline of procedures for the investigation of lymphomas is given to enhance uniformity of interpretation.
Zusammenfassung
Einhundertfünfzig Fälle maligner Lymphome des Tierreiches wurden im Vergleich zu 200 Fällen maligner Lymphome des Menschen nach der modifizierten Rappaportschen Nomenklatur klassifiziert. Der histologische Typ tierischer Lymphome wurde anschließend verglichen mit dem phylogenetischen Stand des Lymphomaträgers, mit dem Wachstumsverhalten des Tumors sowie mit seiner Ätiologie und Pathogenese. Zusätzlich wurden — soweit möglich — immunzytologische Tumorzellbestimmungen durchgeführt.
Es zeigte sich, daß mit wenigen Ausnahmen Tierlymphome auf rein morphologischer Basis nach der Rappaportschen Nomenklatur klassifizierbar waren. Ausnahmen bestanden bei undifferenzierten malignen Lymphomen vom hämozytoblastischen Typ, die beim Menschen nicht beobachtet wurden, und bei hochdifferenzierten lymphozytären Lymphomen, die im Tierreich kaum vorkamen. Weiterhin konnte die angioimmunoblastische Lymphadenopathie des Menschen bisher nicht bei unseren Tieren identifiziert werden und das Retikulumzell-Sarkom Typ B der Maus war beim Menschen nicht in der selben Form vorhanden.
Virus-induzierte Lymphome gehörten überwiegend dem lymphozytären Typ an, während chemisch induzierte oder spontan entstandene Tumoren keine Prädominanz eines bestimmten Zelltypes zeigten. Die beim Menschen beobachtete gesteigerte Häufigkeit von B-Zell-Lymphomen ist im Tierreich nicht in gleicher Weise nachweisbar. Ein bestimmtes, sich wiederholendes Wachstumsmuster fand sich nur bei undifferenzierten Lymphomen vom Burkittoder hämozytoblastischen Typ.
Obgleich das vorhandene Material begrenzt ist, wird doch der Wert zukünftiger einheitlicher Klassifikationen von Tierlymphomen aus der vorliegenden Arbeit ersichtlich.
Similar content being viewed by others
References
Jarret,W.F.H., Mackey,L.J.: II. Neoplastic diseases of the hematopoietic and lymphoid tissues. Bull Wld Hlth Org. 50, 21–34 (1974)
Rappaport,H.: Tumors of the hematopoietic system. Atlas of tumor pathology, Section III- Fascicle 8. Washington D.C.: American Registry of Pathology 1966
Berard,C.W.: Histopathology of the lymphomas. In: Rundles,R.W. (Eds.): Williams,W.J., Beutler,E., Erstlev,A.J., Hematopathology, pp. 901–912. New York: McGraw-Hill Book Co. 1972
Braylan,R.C, Jaffe,E.S. Berard,C.W.: Malignant lymphomas: current classification and new observations. In: Sommers,S.C. (Ed.): Pathology Annual, pp. 213–270. New York: Appleton-Century-Crofts 1975
Sanders,B.J.: Animal histology procedures, DHEW Publication Nr. 72-275, Washington D.C.: U.S. Government Printing Office 1972
Bowling,M.C: Histopathology Laboratory Procedures. DHEW Publication Nr. 1595. Washington D.C.: U.S. Government Printing Office 1967
Pearse,A.G.E.: Histochemistry, p. 886. London: J.A. Churchill Ltd. 1960
Leder,L.D.: Über die selektive fermentcytochemische Darstellung von neutrophilen myeloischen Zellen und Gewebsmastzellen im Paraffinschnitt. Klin. Wschr. 42, 553–555 (1964)
Kaplow,L.S.: Simplified myeloperoxidase stain using benzidine dihydrochloride. Blood 26, 215–219 (1965)
Gomori,G.: An improved histochemical technic for acid phosphatase. Stain Technol. 25, 81–85 (1950)
Gomori,G.: Microtechnical demonstration of phosphatase in tissue sections. Proc. Soc. exp. Biol. (N.Y.) 42, 23–26(1939)
Dunn,T.B.: Deringer,M.K.: Reticulum cell neoplasm, type B, or the “Hodgkin's-like lesion” of the mouse. J. nat. Cancer Inst. 40, 771–821 (1968)
Frizzera,G., Moran,E.M., Rappaport,H., Angio-immunoblastic lymphadenopathy. Diagnosis and clinical course. Amer. J. Med. 59, 803–818 (1975)
Gerard-Marchand,R., Hamlin,I., Lennert.K., Rilke, F., Stansfeld,A.G., Van Unnik,J.A.M: Classification of non-Hodgkin's lymphomas. Letter to the editor. Lancet 1974 II, 406–408
Holmberg,C.A., Manning,J.S., Osburn,B.I.: Canine malignant lymphomas: comparison of morphologic and immunologic parameters. J. nat. Cancer Inst. 56, 125–135 (1976)
Shevach,E.M., Jaffe,E.S., Green,I.: Receptors for complement and immunoglobulin on human and animals lymphoid cells. Transplant. Rev. 16, 3–28 (1973)
Krueger,G., Uhlmann,C., Hellriegel,K.P., Sesterhenn,K., Samii,H., Fischer,R., Wustrow,F., Gross,R.: T- and B-cell receptors in hyperplastic and in neoplastic lesions of the lymphatic system. In: Loeffler,H. (Ed.): Maligne Lymphome und monoklonale Gammopathien, pp. 17–31. Munich: J.F.Lehmanns Verlag 1976
Gleichmann,E., Peters,K., Lattmann,E., Gleichmann,H.: Immunologic induction of reticulum cell sarcoma: donor-type lymphomas in the graft-versus-host model. Europ. J. Immunol. 5, 406–412 (1975)
Hirsch,M.S.: Immunological activation of oncogenic viruses. In: Ceglowski,W.S., Friedman,H. (Eds.): Virus Tumorigenesis and Immunogenesis, pp. 131–137. New York: Academic Press 1973
Preud'Homme,J.L., Seligman,M.: Surface bound immunoglobulins as a cell marker in human lymphoproliferative diseases. Blood 40, 777–794 (1972)
Basten,A., Miller,J.F.A.P., Sprent,J., Pye,J.: A receptor for antibody on B lymphocytes. I. Method of detection and functional significance. J. exp. Med. 135, 610–626 (1972)
Bianco,D.,Patrick,R.,Nussenzweig,V.: A population of lymphocytes bearing a membrane receptor for antigen-antibody-complement complexes. J. exp. Med. 132, 702–720 (1970)
Huber,H., Polley,M.J., Linscott,W.D., Fudenberg,H.H., Muller-Eberhard,H.J.: Human monocytes: distinct receptor sites for the third component of complement and for immunoglobulin G. Science 162, 1281–1283 (1968)
Huber,H., Douglas,S.D., Fudenberg,H.H.: The IgG receptr: an immunological marker for the characterization of mononuclear cells. Immunology 17, 7–21 (1969)
Jondal,M., Holm,G., Wigzell,H.: Surface markers on human T and B lymphocytes. I. A large population of lymphocytes forming non-immune rosettes with sheep red blood cells. J. exp. Med. 136, 207–215 (1972)
Kaplan,M.E., Clark,C: An improved rosetting assay for detection of human T lymphocytes. J. Immunol. Methods 5, 131–135 (1974)
Reif,A.E., Allen,J.M.V.: The AKR thymic antigen and its distribution in leukemias and nervous tissues. J. exp. Med. 120, 413–433 (1964)
Krueger,G., Malmgren,R.A., Berard,C.W.: Malignant lymphomas and plasmacytosis in mice under prolonged immunosuppression and persistent antigenic stimulation. Transplant 11, 138–144 (1971)
Krueger,G., Heine,U.I.: Morphogenesis of two immunologically induced mouse lymphomas. Cancer Res. 32, 573–582 (1972)
Mertens,H., Krueger,G.: Percent distribution of T- and B-lymphoid cells in spleen and lymph nodes of Moloney virus infected mice. Z. Krebsforsch. 85, 169–175 (1976)
Krueger,G., Sesterhenn,K., Uhlmann,C, Ablashi,D.V., Fischer,R., Wustrow,F.: Non-Hodgkin lymphomas: cell populations and their functional behavior. In: Thierfelder,S., Rodth,H., Thiel,E. (Eds.): Immunological Diagnosis of Leukemias and Lymphomas. Munich: J.F.Lehmanns Verlag 1977
Rappaport,H., Braylan,R.C.: Changing concepts in the classification of malignant neoplasms of the hematopoietic system. In: The Reticuloendothelial System, IAP Monograph No. 16, pp. 1–19. Baltimore: Williams & Wilkins 1975
Lukes,R.J., Collins,R.D.: Immunologic characterization of human malignant lymphomas. Cancer 34, 1488–1503 (1974)
Stein,H.: Classification of non-Hodgkin's lymphomas on the basis of morphological and immunological features shared by normal and neoplastic lymphatic cells. Immunität u. Infektion 4, 52–69 (1976)
Bessis,M.: Cellules du sang. Normal et pathologique, p. 673. Paris: Masson & Cie 1972
Dorfman,R.F.: Classification of non-Hodgkin's lymphomas. Lancet 1974 I, 1295–1296
Mathé,G., Rappaport,H., O'Conor,G.T., Torloni,H.: Histological and cytological typing of neoplastic diseases of hematopoietic and lymphoid tissues. International Histological Classification of Tumours, No. 14. Geneva: WHO 1976
Bennet,M.H., Farrer-Brown,G., Henry,K., Jelliffe,A.M.: Classification of non-Hodgkin's lymphomas. Lancet 1974 II, 405–406
Farley,C.A.: Sarcomatoid proliferative disease in a wild population of blue mussels (Mytilusedulis). J. nat. Cancer Inst. 43, 509–516 (1969)
Farley,C.A.: Probable neoplastic disease of the hematopoietic system in oysters, Crassostrea virginica and Crassostrea gigas. Nat. Cancer Inst. Monogr. 31, 541–555 (1969)
Farley,C.A., Sparks,A.K.: Proliferative diseases of hemocytes, endothelial, and connective tissue cells in mollusks, pp. 610–617. Proc. IV. Int. Symp. Comp. Leuk. Res., Dutcher,R.M. (ed.) New York:S.Karger 1971
Oliverio,V.T., O'Gara,R.W.: Reticulum cell sarcoma in a brown shark (Carcharinus milberti). Presented at Workshop on Comparative Pathology of Hematopoietic and Lymphoreticular Neoplasms. Bethesda: National Institutes of Health 1971
Nigrelli,R.F.: Spontaneous neoplasms in fishes III. Lymphosarcoma in Astyanax and Esox. Zoologica 32, 101–108 (1947)
Mulcahy,M.F.: Lymphosarcoma in the pike, Esox lucius L (pisces; esocidae) in Ireland. Proc. R.I.A. 638, 103–129 (1963)
Dunbar,C.E.: Lymphosarcoma of possible thymic origin in salmonid fishes. Nat. Cancer Inst. Monogr. 31, 167–171 (1969)
Smith,C.E.: An undifferentiated hematopoietic neoplasm with histologic manifestations of leukemia in a cutthroat brout (Salmo clarki). J. Fish Res. Bd. Canada 28, 112–113 (1971)
Delanney,L.E., Blackler,K.: Acceptance and regression of a strain-specific lymphosarcoma in Mexican axolotls. In: M.Mizell (Ed.): Biology of Amphibian Tumors, pp. 399–407. Berlin-Heidelberg-New York: Springer 1969
Balls,M.: Spontaneous neoplasms in amphibia: a review and descriptions of six new cases. Cancer Res. 22, 1142–1162 (1962)
Balls, M., Ruben,L.N.: The transmission of lymphosarcoma in Xenopus laevis, the South African clawd toad. Cancer Res. 27, 654–659 (1967)
Frank, W., Schepky, A.: Metatsasizing lymphosarcoma in an anaconda snake, Eunectes murinus (Linnaeus 17581). Path. Vet. 6,437–443 (1969)
Griner,L.A.: Malignant lymphomas in the timber rattle snake and in the death adder. Presented at Workshop on Comparative Pathology of Hematopoietic and Lymphoreticular Neoplasms, Bethesda: National Institutes of Health 1971
Cowan,D.F.: Diseases of captive reptiles. J. Amer. Vet. med. Ass. 153, 848–859 (1968)
Gross,M.A., Burmester,B.R., Walter,W.G.: Pathogenicity of a viral strain (RPL12) causing avian visceral lymphomatosis and related neoplasm. I. Nature of the lesion. J. nat. Cancer Inst. 22, 83–101(1959)
Pontén,J., Burmester,B.R.:Transplantability of primary tumors of RPL12 virus-induced lympoid leukosis. J. nat. Cancer Inst. 38, 505–513 (1967)
Peterson,R.D.A., Purchase,H.C., Burmester,B.R., Cooper,M.D., Good,R.A.: Relationships among visceral lymphomatosis, bursa of Fabricius, and bursa-dependent lymphoid tissue of the chicken. J. nat. Cancer Inst. 36, 585–598 (1966)
Dunn,T.B., Moloney,J.B., Green,A.W., Arnold,B.: Pathogenesis of a virus-induced leukemia in mice. J. nat. Cancer Inst. 26, 189–221 (1961)
Dawe,C.J., Potter,M., Leighton,J.: Progessions of a reticulum cell sarcoma of the mouse in vivo and in vitro. J. nat. Cancer Inst. 21, 753–781 (1958)
Dunn,T.B.: Normal and pathologic anatomy of the reticular tissue in laboratory mice, with a classification and discussion of neoplasms. J. nat. Cancer Instr. 14, 1281–1433 (1954)
Bailey,P.C., Leach,W.B., Hartley,M.W.: Characteristics of a new inbred strain of mice (PBA) with a high tumor incidence: preliminary report. J. Nat. Cancer Inst. 45, 59–73 (1970)
Richter,M.N., Mac Dowell,E.C.: Studies on leukemia in mice. I. The experimental transmission of leukemia. J. expl. Med. 51, 659–673 (1930)
Metcalf,D.: Leukemogenesis in AKR mice. In: Wolstenholme,G.E.W., O'Connor,M. (eds.): CIBA Symposium on Tumour Viruses of Murine Origin. London: Churchill 1962
Kaplan,H.S.: Comparative susceptibility of the lymphoid tissues of strain C57 black mice to the induction of lymphoid tumors by irradiation. J. nat. Cancer Inst. 8, 191–197 (1948)
Krueger,G.: Host response during the latent period and the growth of an immunologically induced mouse lymphoma. Beitr. Path. 146, 132–144 (1972)
Krueger,G., Schaefer,H.E., Luetzeler,J., Fischer,R., Kresin,V.: Spontaneous variations in the cell population of a T-cell lymphoma during tissue culture and transplantation. Z. Krebsforsch. 84, 25–35(1975)
Krueger,G., Harris, D., Sussman,E.: Effect of dilantin in mice. II. Lymphoreticular tissue atypia and neoplasia after chronic exposure. Z. Krebsforsch. 78, 290–302 (1972)
Snell,K. C.: Lymphoblastoma in a rat (J7929). Presented at Workshop on Comparative Pathology of Hematopoietic and Lymphoreticular Neoplasms. Bethesda: National Institutes of Health 1971
Graffi,A.: Wirkungsweise und Eigenschaften des bei der Maus und Ratte wirksamen Virus der myeloischen Leukämie. Acta Unio Int. Contre Cancer 17, 182–197 (1961)
Snell,K. C., Stewart,H.L.: Hematopoietic neoplasms and related conditions in Praomys (Mastomys) natalensis. J. nat. Cancer Inst. 42, 175–202 (1969)
Banfield,W.G.: Hamster lymphoma, TM. nat. Cancer Instr. Monogr. 32, 335–336 (1969)
Schramm,T., Bender,E., Graffi,A.: Leukosis in Syrian hamsters inoculated with hamster papova virus of low titer. Arch. Geschwulst-Forsch. 34, 152–155 (1969)
Graffi,A.,Schramm,T., Bender,E., Graffi,I., Horn,K.H., Bierworf,D.: Cell-free transmissable leukosis in Syrian hamsters, probably of viral aetiology. Brit. J. Cancer 22, 577–581 (1968)
Nielsen,S.W.: Spontaneous hematopoietic neoplasms of the domestic cat. nat. Cancer Inst. Monogr. 32, 73–94 (1969)
Rickard,C.G., Post,J.E., Noronha,F., Barr,L.M.: A transmissable virus-induced lymphocytic leukemia of the cat. J. nat. Cancer Inst. 42,987–1014 (1969)
Squire,R.A.: Spontaneous hematopoietic tumors of dogs. Nat. Cancer Inst. Monogr. 32, 97–115 (1969)
Bloom,F., Meyer,L.M.: Malignant lymphoma (so called leukemia) in dogs. Amer. J. Path. 21, 683–703 (1945)
Monlux,A.W., Anderson,W.A., Davis,C.L.: A survey of tumors occurring in cattle, sheep and swine. Amer. J. Vet. Res. 17, 646–677 (1956)
Smith,H.A.. The pathology of malignant lymphoma in cattle. A study of 1113 cases. Path. Vet. (Basel) 2, 68–93 (1965)
Theilen,G.H., Dungworth,D.L., Lengyel,J., Rosenblatt,L.S.: Bovine lymphosyrcoma in California. I. Epizootiologic and hematologic aspects. Health Lab. Sci. 1, 96–106 (1964)
Migaki,G.: Hematopoietic neoplasms of slaughter animals. Nat. Cancer Inst. Monogr. 32, 121–151(1969)
Griner,L.A.: Reticulum cell sarcoma in a harbor seal (Phoca vitulina geronimensis). Presented at Workshop on Comparative Pathology of Hematopoietic and Lymphoreticular Neoplasms. Bethesda: National Institutes of Health 1971
Lingemann,C.H., Reed,R.E., Garner,F.M.: Spontaneous hematopoietic neoplasms of nonhuman primates. Review, case report and comparative studies. Nat. Cancer Inst. Monogr. 32, 157–170 (1969)
Lapin,B.A., Yakovleva,L.A.: Comparative pathology in monkeys, pp. 176–190. Springfield: Charles C. Thomas 1963
Hunt,R.D., Melendez,L.V., King,N,W., Gilmore,C.E., Daniel,M.D., Williamson,M.E., Jones,T.C.: Morphology of a disease with features of malignant lymphoma in marmosets and owl monkeys inoculated with Herpes saimiri. J. nat. Cancer Inst. 44,447–465 (1970)
Siegal,A.M., Casey,H.W., Bowman,R.W., Traynor,J.E.: Leukemia in a rhesus monkey (Macaca mulatta) following exposure to whole-body proton irradiation. Blood 32,898–966 (1968)
De Paoli,A., Garner,F.M.: Acute lymphocytic leukemia in a white cheeked gibbon (Hylobates concolor). Cancer Res. 28,2559–2561 (1968)
Di Giacomo,R.F.: Burkitt's lymphoma in a white-handed gibbon (Hylobates lar). Cancer Res. 27, 1178–1179 (1967)
Reif,A.E., Allen,J.M.V.: The AKR thymic antigen and its distribution in leukemias and nervous tissues. J. exp. Med. 120, 413–433 (1964)
Shevach,E., Herberman,R., Lieberman,R., Frank,M.M., Green,I.: Receptors for immunoglobulin and complement on mouse leukemias and lymphomas. J. Immunol. 108, 325–328 (1972)
Shevach,E.M., Stobo,J.D., Green,I.: Immunoglobulin and O-bearing murine leukemias and lymphomas. J. Immunol. 108,1146–1151 (1972)
Rouse,B.T., Wells,R.J.H., Warner,L.: Proportion of T and B lymphocytes in lesions of Marek's disease: theoretical implications for pathogenesis. J. Immunol. 110,534–539 (1973)
Haran-Ghera,N., Peled,A.: Thymus and bone marrow derived lymphatic leukaemia in mice. Nature (Lond.) 241, 396–398 (1973)
Shisa,H., Matsudaira,Y., Hiai,H., Nishizuka,Y.: Origin of leukemic cells in mouse leukemia induced by N-nitrosobutylurea. Gann 66, 37–42 (1975)
Hiai,H., Shisa,H., Nishizuka,Y., Miyawaki,H.: An antigen-binding cell tumor: heterophile cold hemagglutinin as a membrane-bound receptor on a mouse lymphoma. J. nat. Cancer Inst. 53, 1703–1711 (1974)
Powell,P.C, Payne,L.N., Frazier,J.A., Rennie,M.: T lymphoblastoid cell lines from Marek's disease lymphomas. Nature (Lond.) 251, 79–80 (1974)
Dawson,P.J., Dresler,S.L., Fieldsteel,A.H.: Immunofluorescence and histologic studies of virus-induced murine lymphocytic leukemias. J. nat. Cancer Inst. 56,1047–1050 (1976)
Merino,F., Abeyounis,C.J., Milgrom,F.: Theta antigen on a murine lymphosarcoma. Transplant Proc. 5,975–976 (1973)
Author information
Authors and Affiliations
Additional information
Part of the work was supported by grant Kr 476/3 of the German Science Foundation
The author gratefully acknowledges helpful advice and discussion of the work by Dr. Costan W.Berard, Dr. Clyde J.Dawe, and Dr. Harold L.Stewart of the National Cancer Institute, USA. The exellent technical and photographic assistance needs also appreciation as done by D. Harris (NCI), B.Koch, B.Raftery, and R.Grossmann (Cologne)
Rights and permissions
About this article
Cite this article
Krueger, G.R.F. Comparative pathologic classification of malignant lymphomas. Z. Krebsforsch. 89, 253–272 (1977). https://doi.org/10.1007/BF00283782
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00283782