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Title: Persistently Infected Horses Are Reservoirs for Intrastadial Tick-Borne Transmission of the Apicomplexan Parasite Babesia equi

Author
item UETI, MASSARO - WSU
item PALMER, GUY - WSU
item Scoles, Glen
item Kappmeyer, Lowell
item Knowles Jr, Donald

Submitted to: Infection and Immunity
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/9/2008
Publication Date: 8/1/2008
Citation: Ueti, M.W., Palmer, G.H., Scoles, G.A., Kappmeyer, L.S., Knowles Jr, D.P. 2008. Persistently Infected Horses Are Reservoirs for Intrastadial Tick-Borne Transmission of the Apicomplexan Parasite Babesia equi. Infection and Immunity. 76(8):3525-3529.

Interpretive Summary: Different species of ticks transmit different pathogens in different ways and the mode of transmission is unique to each different Tick/Pathogen/Host interaction. Some ticks, like the cattle tick Rhipicephalus (Boophilus) microplus, have a life cycle in which all of the life stages (larvae, nymphs and adults) feed on the same host. For these tick species it is not always easy to determine how they transmit a particular pathogen, but an understanding of the possible modes of transmission and their relative efficiencies is essential for development of strategies for controlling transmission. This tick species transmits the protozoan parasite Babesia equi to horses. When horses are acutely infected they have a high level of the parasite in the blood, but after the initial infection horses remain persistently infected for life at a lower level of infection. We tested if adult male ticks could acquire and transmit the pathogen (intrastadial transmission) both during acute and during persistent infection. The level of infection of the horse affected the number of ticks that got infected, but once infected all ticks reached approximately the same level of infection in the salivary glands and were able to successfully transmit. This shows that growth of the parasite in the tick can compensate for initial differences in the dose they receive when feeding on the horse; regardless of dose the parasite can replicate in the salivary glands to a level that exceeds the threshold for transmission. Parasites express different proteins on their surfaces and as part of this work we have shown that the proteins expressed on the cell surface are different in the tick and in the horse, suggesting that the parasite has different mechanisms for survival in the two different environments. Next we tested if female ticks could acquire infection and transmit it through their offspring to a subsequent host (transovarial transmission). Although infection could be detected in a very small proportion of the offspring these offspring were not able to transmit the pathogen when they were allowed to feed through all three life stages on a subsequent host. This study shows that intrastadial transmission, but not transovarial transmission is an efficient mode for B. equi transmission and that persistently infected horses can be an important reservoir for transmission of the parasite. Consequently, strategies to control transmission of this parasite need to target both male ticks and persistently infected horses.

Technical Abstract: Tick-borne pathogens may be transmitted intrastadially and transstadially within a single vector generation as well as vertically between generations. Understanding the mode and relative efficiency of this transmission is required for infection control. In this study, we established that adult male Rhipicephalus microplus ticks efficiently acquire the protozoal pathogen Babesia equi during acute and persistent infection and transmit intrastadially to naïve horses. Although the level of parasitemia during acquisition feeding affected the efficiency of initial tick infection, infected ticks developed levels of ˜10^4 organisms/salivary glands independent of the acquisition parasitemia and successfully transmitted, indicating that replication within the tick compensated for any initial differences in infectious dose and exceeded the threshold for transmission. During the development of B. equi in the salivary gland granular acini, the parasites expressed significantly different levels of paralogous surface proteins as compared to intraerythrocytic parasites from the mammalian host. In contrast to the successful intrastadial transmission, adult female R. microplus ticks acquired B. equi with very low efficiency and passed the parasite vertically into the eggs with similarly low efficiency. The subsequent generation (larvae, nymphs and adults) failed to transmit B. equi to naïve horses. The data demonstrated that intrastadial, but not transovarial, transmission is an efficient mode for B. equi transmission and that persistently infected horses are an important reservoir for transmission. Consequently, control of R. microplus male ticks and persistently infected horses should be targeted for disease control.