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Transstadial and transovarial persistence of Babesia divergens DNA in Ixodes ricinus ticks fed on infected blood in a new skin-feeding technique

  • S. BONNET (a1), M. JOUGLIN (a1), L. MALANDRIN (a1), C. BECKER (a1), A. AGOULON (a1), M. L'HOSTIS (a1) and A. CHAUVIN (a1)...
Abstract

Although Babesia divergens is the the principal confirmed zoonotic Babesia sp. in Europe, there are gaps in our knowledge of its biology and transmission by the tick Ixodes ricinus. In order to reproduce the part of the parasite cycle that occurs in the vector, an in vitro animal skin feeding technique on blood containing in vitro cultivated B. divergens was developed. Parasite DNA was detected in all samples of salivary glands of nymphs and adults that had fed on parasitized blood as larvae and nymphs, respectively, indicating acquisition as well as a transtadial persistence of B. divergens. PCR performed on eggs and larvae produced by females that had fed on parasitized blood demonstrated the existence of a transovarial transmission of the parasite. Gorging B. divergens infected larvae on non-infected gerbils showed persistance of the parasite over moulting into the resulting nymphs. These results indicate that the parasitic stages infective for the vector (i.e. the sexual stages) can be produced in vitro. To our knowledge, this is the first report of artificial feeding of I. ricinus via membrane as well as in vitro transmission of B. divergens to its vector. The opportunities offered by the use of such a transmission model of a pathogen by I. ricinus are discussed.

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Corresponding author
Ecole Nationale Vétérinaire de Nantes, Service de Parasitologie, UMR ENVN/INRA 1034 Interactions Hôte-Parasite-Milieu, Atlanpole-La Chantrerie, B.P. 40706, 44307 Nantes cedex 03, France. Tel: +33 2 40 68 78 58. Fax: +33 2 40 68 77 51. E-mail: bonnet@vet-nantes.fr.
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REFERENCES

Abbassy, M. M., Stein, K. J. and Osman, M. ( 1994). New artificial feeding technique for experimental infection of Argas ticks (Acari: Argasidae). Journal of Medical Entomology 31, 202205.
Bonnet, S., Gouagna, C., Safeukui, I., Meunier, J. Y. and Boudin, C. ( 2000). Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 103106.
Burkot, T. R., Happ, C. M., Dolan, M. C. and Maupin, G. O. ( 2001). Infection of Ixodes scapularis (Acari: Ixodidae) with Borrelia burgdorferi using a new artificial feeding technique. Journal of Medical Entomology 38, 167171.
Chauvin, A., Valentin, A., Malandrin, L. and L'Hostis, M. ( 2002). Sheep as a new experimental host for Babesia divergens. Veterinary Research 33, 429433.
de Moura, S. T., da Fonseca, A. H., Fernandes, C. G. and Butler, J. F. ( 1997). Artificial feeding of Amblyomma cajennense (Fabricius, 1787) (Acari:Ixodidae) through silicone membrane. Memorias do Instituto Oswaldo Cruz 92, 545548.
Donnelly, J. and Peirce, M. A. ( 1975). Experiments on the transmission of Babesia divergens to cattle by the tick Ixodes ricinus. International Journal for Parasitology 5, 363367.
Duh, D., Petrovec, M. and Avsic-Zupanc, T. ( 2001). Diversity of Babesia infecting European sheep ticks (Ixodes ricinus). Journal of Clinical Microbiology 39, 33953397.
Foppa, I. M., Krause, P. J., Spielman, A., Goethert, H., Gern, L., Brand, B. and Telford, S. R. ( 2002). Entomologic and serologic evidence of zoonotic transmission of Babesia microti, in eastern Switzerland. Emerging Infectious Diseases 8, 722726.
Friedhoff, K. T. and Smith, R. D. ( 1981). Transmission of Babesia by ticks. In Babesiosis ( ed. Kreier, M. R. and Kreier, J. P.), pp. 267319. Academic Press, Inc., New York.
Gern, L., Zhu, Z. and Aeschlimann, A. ( 1990). Development of Borrelia burgdorferi in Ixodes ricinus females during blood feeding. Annales de Parasitologie humaine et comparée 65, 8993.
Gorenflot, A., Moubri, K., Precigout, E., Carcy, B. and Schetters, T. P. ( 1998). Human babesiosis. Annals of Tropical Medicine and Parasitology 92, 489501.
Gough, J. M., Jorgensen, W. K. and Kemp, D. H. ( 1998). Development of tick gut forms of Babesia bigemina in vitro. Journal of Eukaryotic Microbiology 45, 298306.
Gray, J., von Stedingk, L. V., Gurtelschmid, M. and Granstrom, M. ( 2002). Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. Journal of Clinical Microbiology 40, 12591263.
Gray, J. S. ( 1980). Studies on the activity of Ixodes ricinus in relation to the epidemiology of babesiosis in Co Meath, Ireland. British Veterinary Journal 136, 427436.
Herwaldt, B. L., Caccio, S., Gherlinzoni, F., Aspock, H., Slemenda, S. B., Piccaluga, P., Martinelli, G., Edelhofer, R., Hollenstein, U., Poletti, G., Pampiglione, S., Loschenberger, K., Tura, S. and Pieniazek, N. J. ( 2003). Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerging Infectious Diseases 9, 942948.
Howarth, J. A. and Hokama, Y. ( 1983). Artificial feeding of adult and nymphal Dermacentor andersoni (Acari: Ixodidae) during studies on bovine anaplasmosis. Journal of Medical Entomology 20, 248256.
Joyner, L. P., Davies, S. F. and Kendall, S. B. ( 1963). The experimental transmission of Babesia divergens by Ixodes ricinus. Experimental Parasitology 14, 367373.
Joyner, L. P. and Purnell, R. E. ( 1968). The feeding behaviour on rabbits and in vitro of the Ixodid tick Rhipicephalus appendiculatus Neumann, 1901. Parasitology 58, 715723.
Kemp, D. H., Koudstaal, D., Roberts, J. A. and Kerr, J. D. ( 1975). Feeding of Boophilus microplus larvae on a partially defined medium through thin slices of cattle skin. Parasitology 70, 243254.
Kjemtrup, A. M. and Conrad, P. A. ( 2000). Human babesiosis: an emerging tick-borne disease. International Journal for Parasitology 30, 13231337.
Kocan, K. M., Holbert, D., Edwards, W., Ewing, S. A., Barron, S. J. and Hair, J. A. ( 1986). Longevity of colonies of Anaplasma marginale in midgut epithelial cells of Dermacentor andersoni. American Journal of Veterinary Research 47, 16571661.
Koch, R. ( 1906). Beiträge zur Entwicklungsgeschichte der Piroplasmen. Zeitschrift für Hygiene und Infektionskrankheiten 54, 19.
Kuhnert, F., Diehl, P. A. and Guerin, P. M. ( 1995). The life-cycle of the bont tick Amblyomma hebraeum in vitro. International Journal for Parasitology 25, 887896.
L'Hostis, M. and Chauvin, A. ( 1999). Babesia divergens in France: descriptive and analytical epidemiology. Parassitologia 41, 5962.
L'Hostis, M., Chauvin, A., Valentin, A., Marchand, A. and Gorenflot, A. ( 1995). Large scale survey of bovine babesiosis due to Babesia divergens in France. Veterinary Record 136, 3638.
Lewis, D. and Young, E. R. ( 1980). The transmission of a human strain of Babesia divergens by Ixodes ricinus ticks. Journal of Parasitology 66, 359360.
Macaluso, K. R., Sonenshine, D. E., Ceraul, S. M. and Azad, A. F. ( 2001). Infection and transovarial transmission of Rickettsiae in Dermacentor variabilis ticks acquired by artificial feeding. Vector Borne and Zoonotic Diseases 1, 4553.
Mackenstedt, U., Gauer, M., Mehlhorn, H., Schein, E. and Hauschild, S. ( 1990). Sexual cycle of Babesia divergens confirmed by DNA measurements. Parasitology Research 76, 199206.
Malandrin, L., L'Hostis, M. and Chauvin, A. ( 2004). Isolation of Babesia divergens from carrier cattle blood using in vitro culture. Veterinary Research 35, 131139.
Mehlhorn, H. and Schein, E. ( 1984). The piroplasms: life cycle and sexual stages. Advances in Parasitology 23, 37103.
Mehlhorn, H., Schein, E. and Voigt, W. P. ( 1980). Light and electron microscopic study on developmental stages of Babesia canis within the gut of the tick Dermacentor reticulatus. Journal of Parasitology 66, 220228.
Meuwissen, J. H. E. T. and Ponnudurai, T. ( 1988). Biology and biochemistry of sexual and sporogonic stages of Plasmodium falciparum: a review. Biology of the Cell 64, 245249.
Mosqueda, J., Falcon, A., Antonio Alvarez, J., Alberto Ramos, J., Oropeza-Hernandez, L. F. and Figueroa, J. V. ( 2004). Babesia bigemina sexual stages are induced in vitro and are specifically recognized by antibodies in the midgut of infected Boophilus microplus ticks. International Journal for Parasitology 34, 12291236.
Musyoki, J. M., Osir, E. O., Kiara, H. K. and Kokwaro, E. D. ( 2004). Comparative studies on the infectivity of Theileria parva in ticks fed in vitro and those fed on cattle. Experimental Applied Acarology 32, 5167.
Purnell, R. E. ( 1970). Infection of the tick Rhipicephalus appendiculatus with Theileria parva using an artificial feeding technique. Research in Veterinary Science 11, 403405.
Purnell, R. E., Young, A. S., Payne, R. C. and Mwangi, J. M. ( 1975). Development of Theileria mutants (Aitong) in the tick Amblyomma variegatum compared to that of T. parva (Muguga) in Rhipicephalus appendiculatus. Journal of Parasitology 61, 725729.
Rechav, Y., Zyzak, M., Fielden, L. J. and Childs, J. E. ( 1999). Comparison of methods for introducing and producing artificial infection of ixodid ticks (Acari: Ixodidae) with Ehrlichia chaffeensis. Journal of Medical Entomology 36, 414419.
Rehacek, J., Sutakoya, G. and Kocianova, E. ( 1994). The use of partially engorged female ticks as laboratory animals in microbiological research. Medical and Veterinary Entomology 8, 165171.
Rudzinska, M. A., Spielman, A., Lewengrub, S., Trager, W. and Piesman, J. ( 1983). Sexuality in piroplasms as revealed by electron microscopy in Babesia microti. Proceeeding of the National Academy of Sciences, USA 80, 29662970.
Stewart, N. P., Dalgliesh, R. J. and De Vos, A. J. ( 1986). Effect of different methods of maintenance on the development and morphology of Babesia bigemina in the gut of Boophilus microplus. Research in Veterinary Science 40, 9498.
Väyrynen, R. and Tuomi, J. ( 1982). Continuous in vitro cultivation of Babesia divergens. Acta Veterinaria Scandinavia 23, 471472.
Voigt, W. P., Young, A. S., Mwaura, S. N., Nyaga, S. G., Njihia, G. M., Mwakima, F. N. and Morzaria, S. P. ( 1993). In vitro feeding of instars of the ixodid tick Amblyomma variegatum on skin membranes and its application to the transmission of Theileria mutans and Cowdria ruminatium. Parasitology 107, 257263.
Waladde, S. M., Young, A. S., Ochieng, S. A., Mwaura, S. N. and Mwakima, F. N. ( 1993). Transmission of Theileria parva to cattle by Rhipicephalus appendiculatus adults fed as nymphae in vitro on infected blood through an artificial membrane. Parasitology 107, 249256.
Wetzel, H. ( 1979). Artificial membrane for in vitro feeding of piercing-sucking arthropods. Entomology Experimental Applications 25, 117119.
Young, A. S., Waladde, S. M. and Morzaria, S. P. ( 1996). Artificial feeding systems for ixodid ticks as a tool for study of pathogen transmission. Annals of the New York Academy of Sciences 791, 211218.
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