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. 1982 Jun;36(3):1060–1068. doi: 10.1128/iai.36.3.1060-1068.1982

Pathogenesis of anemia in Trypanosoma brucei-infected mice.

B O Amole, A B Clarkson Jr, H L Shear
PMCID: PMC551439  PMID: 7201455

Abstract

The pathogenesis of anemia was studied in trypanosome-infected mice. A strain of Trypanosoma brucei, TREU 667, was used which first produces an acute phase marked by waves of parasitemia. Erythrocytes from infected animals were coated with immunoglobulin M during or just before the waves of anemia and parasitological crises. Erythrocytes from normal animals could be sensitized with "precrisis" sera presumably containing antigen and antibody. These data suggest that anemia during the acute phase is due to sensitization of erythrocytes with immunoglobulin M-antigen complexes. The anemia is partially compensated by a strong erythropoietic response. The acute phase is followed by a chronic phase marked by a constant high parasitemia and immunosuppression. The less marked anemia occurring during this latter phase is due to hemodilution and perhaps a low but significant immune response to the parasites, which causes continuing erythrocyte sensitization by immunoglobulin M-antigen complexes.

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Selected References

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  1. Balber A. E. Trypanosoma brucei: attenuation by cortcosteroids of the anemia of infected mice. Exp Parasitol. 1974 Apr;35(2):209–218. doi: 10.1016/0014-4894(74)90024-1. [DOI] [PubMed] [Google Scholar]
  2. Bianco C., Griffin F. M., Jr, Silverstein S. C. Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J Exp Med. 1975 Jun 1;141(6):1278–1290. doi: 10.1084/jem.141.6.1278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brohn F. H., Clarkson A. B., Jr Quantitative effects of salycylhydroxamic acid and glycerol on Trypanosoma brucei glycolysis in vitro and in vivo. Acta Trop. 1978 Mar;35(1):23–33. [PubMed] [Google Scholar]
  4. Brooks B. O., Reed N. D. Trypanosoma musculi: passive hemagglutination technique to measure antibody in mice. Exp Parasitol. 1981 Aug;52(1):49–52. doi: 10.1016/0014-4894(81)90059-x. [DOI] [PubMed] [Google Scholar]
  5. Clarkson A. B., Jr, Brohn F. H. Trypanosomiasis: an approach to chemotherapy by the inhibition of carbohydrate catabolism. Science. 1976 Oct 8;194(4261):204–206. doi: 10.1126/science.986688. [DOI] [PubMed] [Google Scholar]
  6. Cross G. A. Immunochemical aspects of antigenic variation on trypanosomes. The third Fleming Lecture. J Gen Microbiol. 1979 Jul;113(1):1–11. doi: 10.1099/00221287-113-1-1. [DOI] [PubMed] [Google Scholar]
  7. Dargie J. D., Murray P. K., Murray M., Grimshaw W. R., McIntyre W. I. Bovine trypanosomiasis: the red cell kinetics of ndama and Zebu cattle infected with Trypanosoma congolense. Parasitology. 1979 Jun;78(3):271–286. doi: 10.1017/s0031182000051143. [DOI] [PubMed] [Google Scholar]
  8. Diffley P., Strickler J. E., Patton C. L., Waksman B. H. Detection and quantification of variant specific antigen in the plasma of rats and mice infected with Trypanosoma brucei brucei. J Parasitol. 1980 Apr;66(2):185–191. [PubMed] [Google Scholar]
  9. Dodd B. E., Jenkins G. C., Lincoln P. J., McCrorie P. The advantage of a build-up anti-globulin technique for the detection of immunoglobulin on the red cells of rabbits infected with trypanosomes. A preliminary report. Trans R Soc Trop Med Hyg. 1978;72(5):501–505. doi: 10.1016/0035-9203(78)90170-0. [DOI] [PubMed] [Google Scholar]
  10. EDWARDS E. E., JUDD J. M., SQUIRE F. A. Observations on trypanosomiasis in domestic animals in West Africa. III. The haematological changes produced in horses by infections of Trypanosoma vivax, T. congolense and T. brucei. Ann Trop Med Parasitol. 1957 Mar;51(1):63–79. [PubMed] [Google Scholar]
  11. Facer C. A., Bray R. S., Brown J. Direct Coombs antiglobulin reactions in Gambian children with Plasmodium falciparum malaria. I. Incidence and class specificity. Clin Exp Immunol. 1979 Jan;35(1):119–127. [PMC free article] [PubMed] [Google Scholar]
  12. Fruit J., Santoro F., Afchain D., Duvallet G., Capron A. Les immuncomplexes circulants dans la trypanosomiase africaine humaine et expérimentale. Ann Soc Belg Med Trop. 1977;57(4-5):257–266. [PubMed] [Google Scholar]
  13. Huan C. N., Webb L., Lambert P. H., Miescher P. A. Pathogenesis of the anemia in african trypanosomiasis: characterization and purification of a hemolytic factor. Schweiz Med Wochenschr. 1975 Nov 22;105(47):1582–1583. [PubMed] [Google Scholar]
  14. Hudson K. M., Byner C., Freeman J., Terry R. J. Immunodepression, high IgM levels and evasion of the immune response in murine trypanosomiasis. Nature. 1976 Nov 18;264(5583):256–258. doi: 10.1038/264256a0. [DOI] [PubMed] [Google Scholar]
  15. Hudson K. M., Terry R. J. Immunodepression and the course of infection of a chronic Trypanosoma brucei infection in mice. Parasite Immunol. 1979 Winter;1(4):317–326. doi: 10.1111/j.1365-3024.1979.tb00717.x. [DOI] [PubMed] [Google Scholar]
  16. Ikede B. O., Lule M., Terry R. J. Anaemia in trypanosomiasis: mechanisms of erythrocyte destruction in mice infected with Trypanosoma congolense or T. brucei. Acta Trop. 1977 Mar;34(1):53–60. [PubMed] [Google Scholar]
  17. Jayawardena A. N., Waksman B. H. Suppressor cells in experimentally trypanosomiasis. Nature. 1977 Feb 10;265(5594):539–541. doi: 10.1038/265539a0. [DOI] [PubMed] [Google Scholar]
  18. Jennings F. W., Murray P. K., Murray M., Urquhart G. M. Anaemia in trypanosomiasis: studies in rats and mice infected with Trypanosoma brucei. Res Vet Sci. 1974 Jan;16(1):70–76. [PubMed] [Google Scholar]
  19. Kobayashi A., Tizard I. R., Woo P. T. Studies on the anemia in experimental African trypanosomiasis. II. The pathogenesis of the anemia in calves infected with Trypanosoma congolense. Am J Trop Med Hyg. 1976 May;25(3):401–406. doi: 10.4269/ajtmh.1976.25.401. [DOI] [PubMed] [Google Scholar]
  20. Lambert P. H., Berney M., Kazyumba G. Immune complexes in serum and in cerebrospinal fluid in African trypanosomiasis. Correlation with polyclonal B cell activation and with intracerebral immunoglobulin synthesis. J Clin Invest. 1981 Jan;67(1):77–85. doi: 10.1172/JCI110035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laurell C. B. Quantitative estimation of proteins by electrophoresis in agarose gel containing antibodies. Anal Biochem. 1966 Apr;15(1):45–52. doi: 10.1016/0003-2697(66)90246-6. [DOI] [PubMed] [Google Scholar]
  22. Lay W. H., Nussenzweig V. Ca++-dependent binding of antigen-19 S antibody complexes to macrophages. J Immunol. 1969 May;102(5):1172–1178. [PubMed] [Google Scholar]
  23. Lustig H. J., Nussenzweig V., Nussenzweig R. S. Erythrocyte membrane-associated immunoglobulins during malaria infection of mice. J Immunol. 1977 Jul;119(1):210–216. [PubMed] [Google Scholar]
  24. MacKenzie P. K., Cruickshank J. G. Phagocytosis of erythrocytes and leucocytes in sheep infected with Trypanosoma congolense (Broden 1904). Res Vet Sci. 1973 Sep;15(2):256–262. [PubMed] [Google Scholar]
  25. Mackenzie P. K., Boyt W. P., Nesham V. W., Pirie E. The aetiology and significance of the phagocytosis of erythrocytes and leucocytes in sheep infected with Trypanosoma congolense (Broden, 1904). Res Vet Sci. 1978 Jan;24(1):4–7. [PubMed] [Google Scholar]
  26. Mamo E., Holmes P. H. The erythrokinetics of Zebu cattle chronically infected with Trypanosoma congolense. Res Vet Sci. 1975 Jan;18(1):105–106. [PubMed] [Google Scholar]
  27. McCrorie P., Jenkins G. C., Brown J. L., Ramsey C. E. Studies on the anaemia in rabbits infected with Trypanosoma brucei brucei. 2. Haematological studies on the role of the spleen. J Comp Pathol. 1980 Jan;90(1):123–137. doi: 10.1016/0021-9975(80)90034-1. [DOI] [PubMed] [Google Scholar]
  28. Murray M., Murray P. K., Jennings F. W., Fisher E. W., Urquhart G. M. The pathology of Trypanosoma brucei infection in the rat. Res Vet Sci. 1974 Jan;16(1):77–84. [PubMed] [Google Scholar]
  29. Murray P. K., Jennings F. W., Murray M., Urquhart G. M. The nature of immunosuppression in Trypanosoma brucei infections in mice. II. The role of the T and B lymphocytes. Immunology. 1974 Nov;27(5):825–840. [PMC free article] [PubMed] [Google Scholar]
  30. Naylor D. C. The haematology and histopathology of Trypanosoma congolense infection in cattle. I. Introduction and histopathology. Trop Anim Health Prod. 1971;3(2):95–100. doi: 10.1007/BF02356484. [DOI] [PubMed] [Google Scholar]
  31. Poltera A. A., Hochmann A., Rudin W., Lambert P. H. Trypanosoma brucei brucei: a model for cerebral trypanosomiasis in mice--an immunological, histological and electronmicroscopic study. Clin Exp Immunol. 1980 Jun;40(3):496–507. [PMC free article] [PubMed] [Google Scholar]
  32. Preston J. M., Wellde B. T., Kovatch R. M. Trypanosoma congolense: calf erythrocyte survival. Exp Parasitol. 1979 Aug;48(1):118–125. doi: 10.1016/0014-4894(79)90061-4. [DOI] [PubMed] [Google Scholar]
  33. Sacks D. L., Selkirk M., Ogilvie B. M., Askonas B. A. Intrinsic immunosuppressive activity of different trypanosome strains varies with parasite virulence. Nature. 1980 Jan 31;283(5746):476–478. doi: 10.1038/283476a0. [DOI] [PubMed] [Google Scholar]
  34. Sadun E. H., Johnson A. J., Nagle R. B., Duxbury R. E. Experimental infections with African trypanosomes. V. Preliminary parasitological, clinical, hematological, serological, and pathological observations in rhesus monkeys infected with Trypanosoma rhodesiense. Am J Trop Med Hyg. 1973 May;22(3):323–330. doi: 10.4269/ajtmh.1973.22.323. [DOI] [PubMed] [Google Scholar]
  35. Shear H. L., Nussenzweig R. S., Bianco C. Immune phagocytosis in murine malaria. J Exp Med. 1979 Jun 1;149(6):1288–1298. doi: 10.1084/jem.149.6.1288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tartour G., Idris O. F. Iron metabolism in Trypanosoma congolense infection in Zebu cattle: serum iron and serum iron-binding capacity. Res Vet Sci. 1973 Jul;15(1):24–32. [PubMed] [Google Scholar]
  37. Tizard I. R., Holmes W. L., Nielsen K. Mechanisms of the anemia in trypanosomiasis: studies on the role of the hemolytic fatty acids derived from Trypanosoma congolense. Tropenmed Parasitol. 1978 Mar;29(1):108–114. [PubMed] [Google Scholar]
  38. Valli V. E., Forsberg C. M., McSherry B. J. The pathogenesis of Trypanosoma congolense infection in calves. II. Anemia and erythroid response. Vet Pathol. 1978 Nov;15(6):732–745. doi: 10.1177/030098587801500605. [DOI] [PubMed] [Google Scholar]
  39. Valli V. E., Forsberg C. M. The pathogenesis of Trypanosoma congolense infection in calves. V. Quantitative histological changes. Vet Pathol. 1979 May;16(3):334–368. doi: 10.1177/030098587901600307. [DOI] [PubMed] [Google Scholar]
  40. Walia A. S., Shaw D. R., Fuson E. W., Andersson B., Lamon E. W. Different divalent cation requirements for binding IgM complexes to lymphocytes and macrophages. J Exp Med. 1980 Jun 1;151(6):1528–1533. doi: 10.1084/jem.151.6.1528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Weeke B. Rocket immunoelectrophoresis. Scand J Immunol Suppl. 1973;1:37–46. doi: 10.1111/j.1365-3083.1973.tb03777.x. [DOI] [PubMed] [Google Scholar]
  42. Woo P. T., Kobayashi A. Studies on the anaemia in experimental African trypanosomiasis. 1. A preliminary communication on the mechanism of the anaemia. Ann Soc Belg Med Trop. 1975;55(1):37–45. [PubMed] [Google Scholar]
  43. Woodruff A. W. Mechanisms involved in anaemia associated with infection and splenomegaly in the tropics. Trans R Soc Trop Med Hyg. 1973;67(3):313–328. doi: 10.1016/0035-9203(73)90107-7. [DOI] [PubMed] [Google Scholar]
  44. Woodruff A. W., Ziegler J. L., Hathaway A., Gwata T. Anaemia in African trypanosomiasis and 'big spleen disease' in Uganda. Trans R Soc Trop Med Hyg. 1973;67(3):329–337. doi: 10.1016/0035-9203(73)90109-0. [DOI] [PubMed] [Google Scholar]
  45. Worlledge S. M. Immune drug-induced hemolytic anemias. Semin Hematol. 1973 Oct;10(4):327–344. [PubMed] [Google Scholar]

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