Impact of persistent Anaplasma marginale rickettsemia on tick infection and transmission

Abstract

Anaplasma marginale, an intraerythrocytic rickettsia of cattle, is transmitted biologically by ticks. Because of the brevity of acute A. marginale infection, transmission may rely on the tick's ability to acquire the organism from persistently infected cattle with low rickettsemia levels. By using a nucleic acid probe to quantitate low-level infection, we found that rickettsemia levels in persistently infected cattle fluctuated at approximately 5-week intervals during a 24-week period, from <104 infected erythrocytes per ml of blood to high levels of approximately 107 infected erythrocytes per ml of blood. Cattle maintained very low rickettsemia levels (<104.3 infected erythrocytes per ml of blood) for approximately 4 to 8 days of every 5-week cycle. The effect of fluctuations in rickettsemia in persistently infected cattle on acquisition by Dermacentor andersoni nymphal and adult male ticks was examined. A positive correlation was observed between rickettsemia levels in cattle and the resulting infection rates of ticks. At high rickettsemia levels, up to 80% of ticks acquired infection, but even at extremely low rickettsemia levels, 27% of adult male ticks became infected. Moreover, once ticks acquired infection, biological replication of the organism within the ticks appeared to make up for initial differences in the infecting dose. The high infection rates in adult males, combined with their intermittent feeding behavior and the observation that only a few infected ticks were required for transmission to a susceptible host, suggest that adult male D. andersoni ticks are epidemiologically important in A. marginale transmission. Because cattle with all levels of rickettsemia were capable of efficient transmission to ticks, population control efforts must include decreasing transmission from persistently infected individuals.