Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T00:49:13.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of the transmission of Theileria parva between different instars of Rhipicephalus appendiculatus

Published online by Cambridge University Press:  06 April 2009

H. Ochanda ,
A. S. Young ,
C. Wells ,
G. F. Medley  and
B. D. Perry
H. Ochanda*
Affiliation:
International Livestock Research Institute, P.O. Box 30709, Nairobi, Kenya Ecosystems Analysis and Management Group, Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
A. S. Young
Affiliation:
International Livestock Research Institute, P.O. Box 30709, Nairobi, Kenya
C. Wells
Affiliation:
International Livestock Research Institute, P.O. Box 30709, Nairobi, Kenya
G. F. Medley
Affiliation:
Ecosystems Analysis and Management Group, Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK
B. D. Perry
Affiliation:
International Livestock Research Institute, P.O. Box 30709, Nairobi, Kenya
*
* Corresponding author: Department of Zoology, University of Nairobi, P.O. Box 30197, Nairobi, Kenya. Tel: +254 2 445763. Fax: + 254 2 446141. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Summary

The transmission of Theileria parva by nymphal and adult Rhipicephalus appendiculatus was compared by the assessment of salivary gland infections in tick batches fed on the same group of infected cattle at the same time. When larval and nymphal R. appendiculatus Muguga ticks were fed concurrently on cattle undergoing acute infection with T. parva Muguga, the resultant nymphae developed a slightly lower prevalence of infection than did the adult ticks. The abundance of infection was 5–20 times higher in the adult ticks than in the nymphae. When larval and nymphal R. appendiculatus Muguga and R. appendiculatus McIlwaine were fed to repletion on cattle infected with T. parva Boleni, a parasite causing subacute infection, resultant adult tick batches had a relatively high prevalence of infection, but infection was not detected in resultant nymphal batches. When cattle that were carriers of 2 stocks of T. parva, Marikebuni and Kiambu 5, were used as the source of infection, the infections developing in adult R. appendiculatus Muguga ticks were much higher than those developing in nymphae. The structure of salivary glands differed between nymphal ticks, adult males and adult females, and this is considered to be an important factor affecting the infection levels. The morphology of the type III acini, the target acini for sporogony, was similar, but the mean numbers of type III acini were different, with 87 in nymphae, 1346 in males and 1736 in females. This difference was correlated with the different infection levels produced in the various instars and sexes. While the process of sporogony in the different tick instars and sexes was similar, the rate of sporogony was fastest in feeding nymphae, taking on average 2–3 days, compared to 3–4 days in females and an irregular period in the males. These results are discussed in relation to the epidemiology of T. parva.

Keywords

Rhipicephalus appendiculatusTheileria parvatransmissioninfection levelsinstarssalivary gland structure
Type
Research Article
Information
Parasitology , Volume 113 , Issue 3 , September 1996 , pp. 243 - 253
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bailey, K. P. (1960). Notes on the rearing of Rhipicephalus appendiculatus and their infection with Theilera parva for experimental transmission. Bulletin of Epizootic Diseases of Africa 8, 33–43.Google Scholar
Barnett, S. F. (1968). Theileriosis. In Infectious Blood Diseases of Man and Animals, vol. 2 (ed. Weinman, D. & Ristic, M.), pp. 269–328. Academic Press, New York.Google Scholar
Barnett, S. F. & Bailey, K. P. (1955). The infectivity with T. parva of R. appendiculatus fed as larvae and nymphae on cattle reacting to East Coast fever. In East African Veterinary Research Organization. Annual Report 1952–1953: 1954–1955, pp. 66–69. Nairobi: East African High Commission.Google Scholar
Bell, L. J. (1980). Organ culture of Rhipicephalus appendiculatus with maturation of Theileria parva in tick salivary glands in vitro. Acta Tropica 37, 319–325.Google ScholarPubMed
Billingsley, P. F., Medley, G. F., Charlwood, J. D. & Sinden, R. E. (1994). Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 260–270.CrossRefGoogle ScholarPubMed
Binnington, K. C., Young, A. S. & Obenchain, F. D. (1983). Morphology of normal and Theileria parva infected salivary glands of Rhipicephalus appendiculatus (Acari: Ixodoidea). Journal of Parasitology 69, 421–424.CrossRefGoogle ScholarPubMed
Bishop, R., Sohanpal, B., Kariuki, D. P., Young, A. S., Nene, V., Baylis, H., Allsopp, B. A., Spooner, P. R., Dolan, T. T. & Morzaria, S. P. (1992). Detection of a carrier state in Theileria parva-infected cattle by the polymerase chain reaction. Parasitology 104, 215–232.CrossRefGoogle ScholarPubMed
Brocklesby, D. W., Barnett, S. F. & Scott, G. F. R. (1961). Morbidity and mortality rates of East Coast fever (Theileria parva infection) and their application to drug screening procedures. British Veterinary Journal 117, 529–531.CrossRefGoogle Scholar
Büscher, G. & Otim, B. (1986). Quantitative studies on Theileria parva in the salivary glands of Rhipicephalus appendiculatus adults: Quantitation and prediction of infection. International Journal for Parasitology 16, 93–100.CrossRefGoogle ScholarPubMed
Dolan, T. T. (1986). Chemotherapy of East Coast fever: the long term weight changes, carrier state and disease manifestations of parvaquone treated cattle. Journal of Comparative Pathology 96, 137–146.CrossRefGoogle Scholar
Dolan, T. T., Young, A. S., Losos, G. J., McMillan, I., Minder, C. H. E. & Soulsby, K. (1984). Dose dependent responses of cattle to Theileria parva stabilate. International Journal for Parasitology 14, 89–95.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Binnington, K. & Voigt, W. P. (1986). The cell biology of the ixodid tick salivary gland. In Morphology, Physiology and Behavioural Biology of Ticks (ed. Sauer, J. R. & Hair, J. A.), pp. 22–45. Chichester: Ellis Horwood.Google Scholar
Fawcett, D. W., Boscher, G. R. & Doxsey, S. (1982 a). Salivary gland of the tick vector of East Coast fever. IV. Cell type selectivity and host cell responses to Theileria parva. Tissue and Cell 14, 397–414.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Büscher, G. R. & Doxsey, S. (1982 b). Salivary gland of the tick vector of East Coast fever. III. The ultrastructure of the sporogony of Theileria parva. Tissue and Cell 14, 183–206.CrossRefGoogle ScholarPubMed
Fawcett, D. W., Young, A. S. & Leitch, B. L. (1985). Sporogony in Theilera (Apicomplexa: Piroplasmida). A comparative ultrastructural study. Journal of Submicroscopic Cytology 17, 299–314.Google Scholar
Goddeeris, B. M., Katende, J. M., Irvin, A. D. & Chumo, R. S. C. (1982). Indirect fluorescent antibody test for experimental and epizootiological studies on East Coast fever (Theileria parva infection in cattle). Evaluation of a cell culture schizont antigen fixed and stored in suspension. Research in Veterinary Science 33, 360–365.CrossRefGoogle ScholarPubMed
Irvin, A. D., Dobbelaere, D. A. E., Mwamachi, D. M., Minami, T., Spooner, P. R. & Ocama, J. G. R. (1983). Immunization against East Coast fever: Correlation between monoclonal antibody profiles of Theileria parva stocks and cross immunity in vivo. Research in Veterinary Science 35, 341–346.CrossRefGoogle ScholarPubMed
Irvin, A. D., Purnell, R. E., Brown, C. G. D., Cunningham, M. P., Ledger, M. A. & Payne, R. C. (1974). The application of an indirect method of infectivity to ticks with piroplasms for the use in the isolation of field infections. British Veterinary Journal 130, 280–287.CrossRefGoogle ScholarPubMed
Irvin, A. D., Morzaria, S. P., Munatswa, F. C. & Norval, R. A. I. (1989). Immunization of cattle with a Theileria parva bovis stock from Zimbawe protects against challenge with a virulent T. p. parva and T. p. lawrencei stocks from Kenya. Veterinary Parasitology 32, 271–278.CrossRefGoogle Scholar
Jarrett, W. F. H., Crighton, G. W. & Pirie, H. W. (1969). Theileria parva: Kinetics of replication. Experimental Parasitology 24, 9–25.CrossRefGoogle ScholarPubMed
Kamwendo, S. P., Ingram, G. A., Musisi, F. L., Trees, A. J. & Molyneux, D. H. (1993). Characteristics of tick, Rhipicephalus appendiculatus, glands distinguished by surface lectin binding. Annals of Tropical Medicine and Parasitology 87, 525–535.CrossRefGoogle ScholarPubMed
Koch, H. T. (1990). Aspects of the epidemiology of January disease (Theileria parva bovis infection) in Zimbabwe. Ph.D. thesis, University of Utrecht.Google Scholar
Koch, H. T., Kambeva, L., Norval, R. A. I., Ocama, J. G. R. & Munatswa, F. C. (1993). Transmission of Theileria parva bovis by nymphs of Rhipicephalus appendiculatus. Preventive Veterinary Medicine 17, 89–93.CrossRefGoogle Scholar
Lawrence, J. A. & Mackenzie, P. K. I. (1980). Isolation of a non-pathogenic Theileria of cattle transmitted by Rhipicephalus appendiculatus. Zimbabwe Veterinary Journal 11, 27–35.Google Scholar
Lawrence, J. A., Norval, R. A. I. & Uilenberg, G. (1983). Rhipicephalus Zambeziensis as a vector of bovine theileriae. Tropical Animal Health and Production 15, 39–42.CrossRefGoogle ScholarPubMed
Lounsbury, C. P. (1904). Transmission of African Coast fever. Agricultural Journal of Cape of Good Hope 24, 428–432.Google Scholar
Martin, H. M., Barnett, S. F. & Vidler, B. O. (1964). Cyclic development and longevity of Theileria parva in the tick Rhipicephalus appendiculatus. Experimental Parasitology 15, 527–555.CrossRefGoogle ScholarPubMed
Medley, G. F., Perry, B. D. & Young, A. S. (1993 a). Preliminary analysis of the transmission dynamics of Theileria parva in eastern Africa. Parasitology 106, 251–264.CrossRefGoogle ScholarPubMed
Medley, G. F., Sinden, R. E., Fleck, S., Billingsley, P. F., Tirawanchai, N. & Rodriguez, M. H. (1993 b). Heterogeneity in Patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–449.CrossRefGoogle ScholarPubMed
Minami, T., Spooner, P. R., Irvin, A. D., Ocama, J. G. R., Dobbelaere, D. A. E. & Fujinaga, T. (1983). Characterization of stocks of Theileria parva by monoclonal antibody profiles. Research in Veterinary Science 35, 334–340.CrossRefGoogle ScholarPubMed
Norval, R. A. I., Fivaz, B. H., Lawrence, J. A. & Brown, A. F. (1985). Epidemiology of tick-borne disease of cattle in Zimbabwe. III. Theileria parva group. Tropical Animal Health and Production 17, 19–28.CrossRefGoogle ScholarPubMed
Pegram, R. G., James, A. D., Bamhare, C., Dolan, T. T., Hove, T., Kanhai, G. K. & Latif, A. A. (1996). Effects of immunization against Theileria parva on beef cattle productivity and economics of control options. Tropical Animal Health and Production (in the Press.)CrossRefGoogle Scholar
Perry, B. D., Deem, S. L., Medley, G. F., Morzaria, S. P. & Young, A. S. (1992). The ecology of Theileria parva infections of cattle and the development of endemic stability. In The Proceedings of First Conference on Tick-borne Pathogens at the Host-Vector Interface, (ed. Munderloh, U. G. & Kurtti, T. J.), pp. 290–296. University of Minnesota, Saint Paul.Google Scholar
Purnell, R. E. & Joyner, L. P. (1968). The development of Theileria parva in the salivary glands of the tick, Rhipicephalus appendiculatus. Parasitology 58, 725–732.CrossRefGoogle ScholarPubMed
Purnell, R. E., Boarer, C. D. H. & Pierce, M. A. (1971). Theileria parva: Comparative infection rates of adult and nymphal Rhipicephalus appendiculatus. Parasitology 62, 349–353.CrossRefGoogle ScholarPubMed
Purnell, R. E., Young, A. S., Brown, C. G. D., Burridge, M. J. & Payne, R. C. (1974). Comparative infectivity for cattle of stabilates of Theileria lawrencei (Serengeti) derived from adults and nymphal ticks. Journal of Comparative Pathology 84, 533–537.CrossRefGoogle ScholarPubMed
Radley, D. E., Brown, C. G. D., Burridge, M. J., Cunningham, M. P., Pierce, M. A. & Purnell, R. E. (1974). East Coast fever: Quantitative studies of Theileria parva in cattle. Experimental Parasitology 36, 278–287.CrossRefGoogle ScholarPubMed
Reichenow, E. (1940). Der Entwicklungsgang des Kustenfiebererreges in Rinde und in der ubertragenden Zeche. Archiv für Protistenkunde 94, 1–56.Google Scholar
Shaw, M. K., Tilney, L. G. & Musoke, A. J. (1991). The entry of Theileria parva sporozoites into bovine lymphocytes: Evidence for MHC involvement. Journal of Cell Biology 113, 87–101.CrossRefGoogle Scholar
Shaw, M. K. & Young, A. S. (1995). Differential development and emission of Theileria parva sporozoites from the salivary glands of Rhipicephalus appendiculatus. Parasitology 111, 153–160.CrossRefGoogle ScholarPubMed
Short, N. J. & Norval, R. A. I. (1981). The seasonal activity of Rhipicephalus appendiculatus Neumann 1901 (Acarina: Ixodidae) in the highveld of Zimbabwe Rhodesia. Journal of Parasitology 67, 77–84.CrossRefGoogle ScholarPubMed
Sonenshine, D. E. (1991). Biology of Ticks, vol. 1. Oxford University Press; New York.Google Scholar
Theiler, A. (1905). Report of the Government Veterinary Bacteriologist 1904–5. in Transvaal Department of Agriculture. Annual Report of the Director of Agriculture, 1906, pp. 75–187. Pretoria: Government Printing and Stationary Office.Google Scholar
Uilenberg, G., Perie, N. M., Lawrence, J. A., De Vos, A. J., Paling, R. W. & Spanjer, A. A. M. (1982). Causal agents of bovine theileriosis in southern Africa. Tropical Animal Health and Production 14, 127–140.CrossRefGoogle ScholarPubMed
Voigt, W. P., Mwaura, S. N., Njihia, G. M., Nyaga, S. G. & Young, A. S. (1995). Detection of Theileria parva in the salivary glands of Rhipicephalus appendiculatus: evaluation of staining methods. Parasitology Research 81, 74–81.CrossRefGoogle ScholarPubMed
Warburg, A. & Miller, L. H. (1991). Critical stages in the development of Plasmodium in mosquitoes. Parasitology Today 7, 179–181.CrossRefGoogle ScholarPubMed
Young, A. S. & Leitch, B. L. (1981). Epidemiology of East Coast fever. Some effects of temperature on the development of Theileria parva in the tick vector, Rhipicephalus appendiculatus. Parasitology 83, 199–211.CrossRefGoogle ScholarPubMed
Young, A. S., Leitch, B. L., Newson, R. M. & Cunningham, M. P. (1986). Maintenance of Theileria parva parva infection in an endemic area of Kenya. Parasitology 93, 9–16.CrossRefGoogle Scholar
Young, A. S., Leitch, B. L., Stagg, D. A. & Dolan, T. T. (1983). Identification of Theileria infection in living salivary glands of ticks. Parasitology 86, 519–528.CrossRefGoogle Scholar