Skip to main content

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

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

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

    Google Scholar 

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

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

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

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1186/BF03548606

Keywords

  • inverse age resistance
  • IgM
  • IgG antibodies