Transmission Dynamics of Borrelia turicatae from the Arthropod Vector

Abstract

Background

With the global distribution, morbidity, and mortality associated with tick and louse-borne relapsing fever spirochetes, it is important to understand the dynamics of vector colonization by the bacteria and transmission to the host. Tick-borne relapsing fever spirochetes are blood-borne pathogens transmitted through the saliva of soft ticks, yet little is known about the transmission capability of these pathogens during the relatively short bloodmeal. This study was therefore initiated to understand the transmission dynamics of the relapsing fever spirochete Borrelia turicatae from the vector Ornithodoros turicata, and the subsequent dissemination of the bacteria upon entry into murine blood.

Methodology/Principal Findings

To determine the minimum number of ticks required to transmit spirochetes, one to three infected O. turicata were allowed to feed to repletion on individual mice. Murine infection and dissemination of the spirochetes was evaluated by dark field microscopy of blood, quantitative PCR, and immunoblotting against B. turicatae protein lysates and a recombinant antigen, the Borrelia immunogenic protein A. Transmission frequencies were also determined by interrupting the bloodmeal 15 seconds after tick attachment. Scanning electron microscopy (SEM) was performed on infected salivary glands to detect spirochetes within acini lumen and excretory ducts. Furthermore, spirochete colonization and dissemination from the bite site was investigated by feeding infected O. turicata on the ears of mice, removing the attachment site after engorment, and evaluating murine infection.

Conclusion/Significance

Our findings demonstrated that three ticks provided a sufficient infectious dose to infect nearly all animals, and B. turicatae was transmitted within seconds of tick attachment. Spirochetes were also detected in acini lumen of salivary glands by SEM. Upon host entry, B. turicatae did not require colonization of the bite site to establish murine infection. These results suggest that once B. turicatae colonizes the salivary glands the spirochetes are preadapted for rapid entry into the mammal.

Author Summary

Relapsing fever spirochetes cause recurrent febrile episodes, rigors, nausea, vomiting, malaise, and pregnancy complications, and are a leading cause of hospital admissions in regions of Africa. Routes of pathogen transmission include crushed human body lice and feces, or through bites by Ornithodoros spp. of ticks. The life cycle of Ornithodoros turicatae, the vector of Borrelia turicatae, includes over six nymphal stages, upwards of a ten year life span, and a bloodmeal that is completed within an hour. We investigated B. turicatae transmission from the tick vector and assessed the rapidity of spirochete entry into the mammal and dissemination in the blood. Salivary glands from infected ticks were also evaluated to visualize B. turicatae within the tissues to determine spirochete localization. We conclude that given the transmission dynamics of B. turicatae, it may be important to target conserved surface proteins that relapsing fever spirochetes produce in the salivary glands in order to develop preventative measures against the pathogens.