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Clinical and Serological Response after Experimental Inoculation with Babesia Divergens of Newborn Calves with and without Maternal Antibodies

Experimentell infektion med Babesia divergens av nyfödda kalvar med och utan maternala antikroppar

Acta Veterinaria Scandinavica volume 28, pages381–392(1987)Cite this article

Abstract

The influence of maternal antibodies on clinical and serological response after experimental inoculation with Babesia divergens of newborn calves was studied. Five calves, born to dams seropositive for B.divergens, (Group 1) had specific maternal antibodies when tested 12 h after their first feeding of colostrum. At that point they were inoculated i.v. with B.divergens infected erythrocytes. Five other calves, born to dams seronegative for B.divergens, (Group 2) had no Babesia specific maternal antibodies when inoculated at the same age.

Babesia divergens organisms were demonstrated in blood smears from calves in both groups at some point 5 to 10 days p.i. All calves in both groups had B.divergens specific IgM antibodies at 7 to 17 days p.i. as shown by a modified IF-test. Specific IgG antibodies, transferred by colostrum, were found in all calves of Group 1 before inoculation of B.divergens. The IgG titre of these animals increased by a doubling dilution step at 11–25 days p.i. Among calves of Group 2 specific IgG antibodies were found at first between day 9 and 15 p.i. Both IgM and IgG antibody titres had to be investigated since demonstrated IgG antibodies can originate both from maternally transferred antibodies and from actively produced antibodies after an infection.

There was no difference in clinical parameters; parasitaemia, PCV, Hb, and rectal temperature between the groups.

This experiment gives evidence that there can be a resistance to bovine babesiosis in newborn calves independent of maternal antibodies.

Sammanfattning

Omvänd åldersresistens hos nötkreatur mot infektion med Babesia-arter är ett sedan länge observerat fenomen vars natur är oklar. Maternalt överförda antikroppar har av några författare ansetts kunna vara orsak till resistensen hos kalvar, åtminstone under de 2 första levnadsmånaderna. För att studera betydelsen av maternalt överförda specifika antikroppar infekterades 2 grupper nyfödda kalvar om 5 djur i vardera gruppen med B.divergens. Djuren i båda grupperna infekterades av en Babesiastam som visats kunna ge klinisk babesios hos splenektomerade kalvar. Den ena gruppen hade maternala, med råmjölken överförda, specifika antikroppar. Den andra gruppen fick råmjölk från kor utan antikroppar mot B.divergens. Parasitemi, hematokrit, Hb och rektal-temperatur mättes. Serologiskt undersöktes förekomst av specifika IgM och IgG antikroppar med en modifierad IF-teknik. Med hjälp av den tidpunkt då IgM antikroppar började uppträda kunde antikroppsförekomst orsakad av Babesia infektion hos kalven särskiljas från maternala, passivt överförda specifika IgG antikroppar.

Kalvarna i båda grupperna blev infekterade, men inga djur reagerade kliniskt efter infektionen. Specifika IgM antikroppar påvisades hos kalvar från båda grupperna 7–17 dagar efter infektion. Specifika IgG antikroppar påvisades från början hos kalvar med maternala antikroppar och 9–15 dagar efter infektion hos kalvar utan maternala antikroppar. Vid motsvarande tidpunkt sågs en titerstegring av IgG hos kalvar med maternala antikroppar. Inga andra skillnader mellan grupperna iakttogs. Infekterade nyfödda kalvar kan bli kroniska smittbärare av B.divergens, vilket visades genom splenektomi av en kalv 5 månader efter infektionen.

Denna undersökning visar att det finns en resistens mot B.divergens hos späda kalvar, vilken är oberoende av specifika maternala antikroppar.

References

  1. Aalund O: Heterogeneity of ruminant immunoglobulins. Thesis Munksgaard, Copenhagen, 1968.

    Google Scholar 

  2. Aragon R S: Bovine babesiosis: A review. Vet. Bull. 1976,46, 903–917.

    Google Scholar 

  3. Berry S, Ibata G, Edwards S: Antibody formation to Babesia bovis and Anaplasma marginale in calves in Bolivia. Trop. Anim. Health Prod. 1981,13, 240–241.

    CAS  PubMed  Article  Google Scholar 

  4. Bidwell DE, Turp P, Joyner L P, Payne R C, Purnell R E: Comparisons of serological tests for Babesia in British cattle. Vet. Rec. 1978,103, 446–449.

    CAS  PubMed  Article  Google Scholar 

  5. Butler, J E: Immunoglobulins of the mammary secretions In: Lactation a omprehensive Treatise Vol. III, Ed. Larsson, L. & Smith, V., Academic Press, London, 1974, p. 217–255.

    Google Scholar 

  6. Callow L L: Strain immunity in babesiosis. Nature 1964,204, 1213–1214.

    CAS  PubMed  Article  Google Scholar 

  7. Callow L L: Sterile immunity, coinfectious immunity and strain differences in Babesia bigemina infections. Parasitology 1967,57, 455–465.

    CAS  PubMed  Article  Google Scholar 

  8. Callow L L: A note on homologous strain immunity in Babesia argentina infections. Aust. Vet. J. 1968,44, 268–269.

    CAS  PubMed  Article  Google Scholar 

  9. Callow L L: Vaccination against bovine babesiosis. In: Immunity to blood parasites of animals and man. Ed. L. H. Miller, J. A. Pino & J. J. McKel–vey Jr. Advances in experimental Medicine and Biology. Plenum Press, New York. Vol. 93, 1977, p. 121–150.

    CAS  Article  Google Scholar 

  10. Callow LL, Pepper Ρ M: Measurement of and correlations between fever changes in the packed cell volume and parasitaemia in the evaluation of the susceptibility of cattle to infection with Babesia argentina. Aust. Vet. J. 1974,50, 1–5.

    CAS  PubMed  Article  Google Scholar 

  11. Callow L L, Dalgliesh R J: Immunity and immuno–pathology in babesiosis. In: Immunology of Parasitic Infections. Ed. S. Cohen & K. Warren. Blackwell cientific Publications, Oxford, 1982, p. 475–526.

    Google Scholar 

  12. Christensson D A: A modified IF-test to demonstrate IgM antibodies to Babesia divergens of cattle. Acta vet. scand. 1987, 28, 361–371

    CAS  PubMed  Article  Google Scholar 

  13. Christensson D A, Thorburn M: Age distribution of natural occurring acute babesiosis in cattle in Sweden. Acta vet. scand. 1987, 28

  14. Cox F E G, Turner S A: Antibody levels in mice infected with Babesia microti. Ann. trop. Med. Pa–rasit. 1970,64, 164–173.

    Google Scholar 

  15. Curnow J A: In vitro agglutination of bovine erythrocytes infected with Babesia argentina. Nature 1968,217, 267–268.

    CAS  PubMed  Article  Google Scholar 

  16. Curnow J A: Studies on the antigenic changes and strain differences in Babesia argentina infections. Aust. Vet. J. 1973,49, 279–283.

    CAS  PubMed  Article  Google Scholar 

  17. Dalgliesh R J: Theoretical and practical aspect of freezing parasite protozoa. Aust. Vet. J. 1972,48, 233–239.

    CAS  PubMed  Article  Google Scholar 

  18. Dalgliesh R J, Mellors L T: Survival of the parasitic protozoan Babesia bigemina in blood cooled at widely different rates to–196°C. Int. J. Parasi–tol. 1974,4, 169–172.

    CAS  Article  Google Scholar 

  19. O’Donoghue Ρ J, Friedhoff Κ Τ, Kizcaino Ο G, Weyreter H: The detection of IgM and IgG antibodies against Babesia bigemina in bovine sera using semi–defined antigens in enzyme immunoassays. Vet. Parasitol. 1985,18, 1–12.

    PubMed  Article  Google Scholar 

  20. Goff L W, Wagner G G, Craig T M, Long R F: The immune response to tick derived Babesia bovis infection: Serological studies of isolated immunoglobulins. Vet. Parasitol. 1982,11, 109–120.

    CAS  PubMed  Article  Google Scholar 

  21. Hall W Τ Κ: The immunity to Babesia argentina infection. Aust. Vet. J. 1960,36, 361–366.

    Article  Google Scholar 

  22. Hall W T K: The immunity of calves to tick–transmitted Babesia argentina infection. Aust. Vet. J. 1963,39, 386–389.

    Article  Google Scholar 

  23. Hall W T K, Tammemagi L, Johnston L A Y: Bovine babesiosis: The immunity of calves to Babesia bigemina infection. Aust. Vet. J. 1968,44, 259–264.

    CAS  PubMed  Article  Google Scholar 

  24. Hopps D C: An evaluation of colostral immunity and the acquired immune response to bovine babesiosis using the complement fixation and the indirect fluorescent antibody test. Diss. Abstr. Inst. 1977, 37B, 3806–3807.

    Google Scholar 

  25. Hyrenius H: Statistiska metoder (Statistical Methods). Gumperts, Göteborg 1962, p. 407–411.

    Google Scholar 

  26. Joyner L P, Donnelly J: The epidemiology of babe–sial infections. In: Advances in Parasitology. Vol. 17, Ed. Lumsden, W H.R., Muller, R. & R. J. Baker, Academic Press, London 1979, p. 49–113.

    Article  Google Scholar 

  27. Klaus G G B, Bennet A, Jones Ε W: A quantitative study of the transfer of colostral immunoglobulins of the newborn calf. Immunology 1969,16, 293–299.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Latif, B M A, Said M S, Ali S R: Effect of age on the immune response of cattle infected with Babesia bigemina. Vet. Parasitol. 1979,5, 307–314.

    Article  Google Scholar 

  29. Legg J: A brief review of the piroplasms with special reference to the types found in Australian »red–water«. Aust. Vet. J. 1933,9, 14–19.

    Article  Google Scholar 

  30. Levy Μ G, Clabaugh G, Ristic M: Age resistance in bovine babesiosis: role of blood factors in resistance to Babesia bovis. Infec. & Immunity. 1982,37, 1127–1131.

    CAS  Article  Google Scholar 

  31. Mahoney D F: Bovine babesiosis: the passive immunization of calves against Babesia argentina with special reference to the role of complement fixing antibodies. Exp. Parasitol. 1967,20, 119–124.

    CAS  PubMed  Article  Google Scholar 

  32. Mahoney D F: Immune response to haemoprotozoa II. Babesia spp. In: Immunity to Animal Parasites, Ed. Soulsby, E. J. L., Academicms, London, 1972, p. 301–341.

    Google Scholar 

  33. Mahoney D F: Studies on the protection of cattle against Babesia bovis infection. In: Ed: Dunsmo–re, J. D., 10th Meeting, World Assoc. Adv. Parasitol. Perth, August 1983, p. 93–104.

  34. Mahoney D F, Goodger Β V: Babesia argentina: im-munogenicity of plasma from infected animals. Exp. Parasitol. 1972,32, 71–85.

    CAS  PubMed  Article  Google Scholar 

  35. Murphy F A O, Aalund O, Osebold J W, Carroll Ε J: Gamma globulins of bovine secretion. Archs Biochem. Biophys. 1964,108, 230–239.

    CAS  Article  Google Scholar 

  36. Phillips R S: The protective activity of serum from immune rats against Babesia rodhaini. Parasitology, 1969,59, 357–364.

    CAS  PubMed  Article  Google Scholar 

  37. Phillips R S: Evidence that piroplasms can undergo antigenic variation. Nature 1971, 231, 323.

    CAS  PubMed  Article  Google Scholar 

  38. Pierce E E, Feinstein A: Biophysical and immunological studies on bovine immunoglobulins with evidence for selective transport within the mammary gland from maternal plasma colostrum. Immunology, 1965,8, 106–123.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Pipano E: Immunization of cattle against Babesiella berbera infection I. Infection of cattle with blood from patent and latent carriers. Refuah Vet. 1969,26, 11–18.

    Google Scholar 

  40. Purnell R E, Brocklesby D W, Kitchenham Β A, Young Ε R: A statistic comparison of the behaviour of five British isolates of Babesia divergens in splenectomized calves. J. Comp. Path. 1976,86, 609–614.

    CAS  PubMed  Article  Google Scholar 

  41. Riek R F: Babesiosis. In: Infectious Blood Diseases of Man and Animals, Ed. Wienman, D. & M. Ristic, Academics, London 1968, p. 246–248.

    Google Scholar 

  42. Ross J Ρ J, Löhr Κ F: Ubertragung und Verweil–dauer von kolostral erworbenen Babesia bigemi–na und Anaplasma marginale–Antikorpern. (Transmission and duration of colostral derived antibodies to B.divergens and A.marginale). Z. tropenmed. Parasit. 1970,21, 401–411.

    CAS  Google Scholar 

  43. Schalm Ο W: The blood and blood forming organs. In: Bovine Medicine and Surgery, Ed. Gibbons, W. J., E. J. Catcott & J. F. Smithcors. Am. Vet. Publi. Inc. 1970, p. 519–546.

    Google Scholar 

  44. Smith T, Kilborne F L: Investigations into the nature, causation and prevention of Texas and Southern cattle fever. U.S. Dep. Agric. Bur. Anim. Ind., Bull. no. 1, 1893, 1–301.

    Google Scholar 

  45. Solomon J B: Fetal and neonatal immunology. Frontiers of Biology Series. Vol. 20, Elsevier. North Holland, New York 1971.

  46. Staley T E, Jones Ε W, Bush L J: Maternal transport of immunoglobulins to the calf. J. Dairy Sci. 1971, 54, 1323.

    CAS  PubMed  Google Scholar 

  47. Taylor S M, Kenny J, Mallon T: The effect of multiple passage on strains of Babesia divergens. A comparison of the clinical effects on juvenile and adult cattle of passaged and irradiated parasites. J. Comp. Pathol. 1983,93, 391–396.

    CAS  PubMed  Article  Google Scholar 

  48. Trees A J: The application of acridine orange staining to quantitate low levels of Babesia divergens parasitaemias. Trans. R. Soc. trop. Med. Hyg. 1974, 68, 277.

    CAS  PubMed  Google Scholar 

  49. Trueman H F, Blight G W: The effect of age on resistance of cattle to Babesia bovis. Aust. Vet. J. 1978,54, 301–305.

    CAS  PubMed  Article  Google Scholar 

  50. Uilenberg G: Notes sur les babesioses et l’anaplas–mose des bovins à Madagascar V. A. Immunité et prémunition. B. Epizootologie (Notes on the babesiosis and the anaplasmosis of bovines on Madagascar V. A. Immunity and premunition. B. Epizootiology. Revue Elev. Méd. vét. Pays trop. 1970,23, 439–454.

    CAS  Article  Google Scholar 

  51. Uilenberg G: Notes sur les babesioses et l’anaplas–mose des bovins à Madagascar VI. Prémunition artificielle (Notes on babesiosis and anaplasmosis of bovines in Madagascar VI. Artificial premunition). Revue Elev. Med. vet. Pays trop. 1971,24, 23–35.

    CAS  Article  Google Scholar 

  52. Weisman J, Goldman M, Mayer E, Pipano E: Passive transfer to newborn calves of maternal antibodies against Babesia bigemina and Babesia berbera. Refuah Vet. 1974,31, 108–113.

    Google Scholar 

  53. Wahlgren M, Christensson D, Bergquist R, Björk–man A, Pehrsson P-O, Rombo L: Babesios, en risksjukdom för immunodefekta i Sverige (Babesiosis, a disease at risk for people with immunodeficiency in Sweden). Opusc. med. 1984,29, 26–28.

    Google Scholar 

  54. Winter Η: Staining with acridin orange, res. Vet. Sci. 1967, 8, 170.

    CAS  Article  Google Scholar 

  55. Zwart D: Haemoparasitic diseases of bovines. O.I. E.-review 1985.

    Google Scholar 

  56. Zwart D, Brocklesby D W: Babesiosis: non–specific resistance, immunological factors and pathogenesis. In: Advances in Parasitology. Vol. 17, Ed. Lumsden, W. H. R., R. Muller & R. J. Baker, Academic Press, London, 1979, p. 49–113.

    CAS  PubMed  Article  Google Scholar 

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Acknowledgment

Among the persons who made this experiment possible, I especially want to thank Dr. T. Morén for producing fresh strains of B.divergens, Professor P. Holtenius and his staff for providing calves and free access to the facilities at the Department of Cattle and Sheep Diseases, Professor O. Holmberg for providing newborn calves, Ms. E. Orstadius and Ms. K. Candelöf for technical assistance and Ms. G. Wikne for typing the manuscript.

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  1. Department of Veterinary Microbiology, Section of Parasitology, Swedish University of Agricultural Sciences and National Veterinary Institute, P. O. Box 7073, S-75007, Uppsala, Sweden

    Dan A. Christensson

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Correspondence to Dan A. Christensson.

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Christensson, D.A. Clinical and Serological Response after Experimental Inoculation with Babesia Divergens of Newborn Calves with and without Maternal Antibodies. Acta Vet Scand 28, 381–392 (1987). https://doi.org/10.1186/BF03548606

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Keywords

  • inverse age resistance
  • IgM
  • IgG antibodies

Acta Veterinaria Scandinavica

ISSN: 1751-0147

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