Investigations on the Mode and Dynamics of Transmission and Infectivity of <i>Borrelia burgdorferi</i> Sensu Stricto and <i>Borrelia afzelii</i> in <i>Ixodes ricinus</i> Ticks

<i>Borrelia burgdorferi</i> sensu lato (sl), the agent of Lyme disease, is transmitted to the host during the blood meal of <i>Ixodes</i> ticks. In most unfed ticks, spirochetes are present in the midgut and migrate during blood feeding to the salivary glands, from which they are transmitted to the host via saliva. In the present study, the efficiency of <i>Ixodes ricinus</i> ticks to transmit <i>B. afzelii</i> and <i>B. burgdorferi</i> sensu stricto (ss) and their infectivity for mice were examined in relation to the duration of the blood meal. In addition, we investigated whether these two <i>Borrelia</i> species can penetrate intact skin. Three modes of infection of mice were studied: tick-bite infection, inoculation of tick homogenates, and transcutaneous infection by topical application of tick homogenates on mouse skin. Transmission of <i>B. burgdorferi</i> sl from <i>I. ricinus</i> nymphs to mouse increased with duration of tick attachment. <i>B. afzelii</i>-infected ticks start to transmit infection earlier (≤48 h) than <i>B. burgdorferi</i> ss-infected ticks. As previously shown for <i>B. burgdorferi</i> ss in <i>Ixodes scapularis</i>, <i>B. burgdorferi</i> ss and <i>B. afzelii</i> in unfed <i>I. ricinus</i> were noninfectious for mice when tick homogenates were inoculated. However, the inoculation of homogenates of ticks fed for 24 h readily produced infection in mice. Therefore, <i>B. burgdorferi</i> ss and <i>B. afzelii</i> spirochetes are potentially infectious in the tick before natural transmission can occur. None of the mice (<i>n</i> = 33) became infected by transcutaneous transmission when tick homogenates were applied on mouse skin, showing that <i>B. burgdorferi</i> ss and <i>B. afzelii</i> are unable to penetrate intact skin, in contrast to relapsing fever spirochetes. This study also shows that <i>B. afzelii</i> is transmitted by <i>I. ricinus</i> to the host earlier than <i>B. burgdorferi</i> ss and that <i>I. ricinus</i> seems to be a more efficient vector of <i>B. afzelii</i> than <i>B. burgdorferi</i> ss.