Abstract

The γ-proteobacterium Francisella tularensis causes seasonal tick-transmitted tularemia outbreaks in natural rabbit hosts and incidental infections in humans in the south-central United States. Although Dermacentor variabilis is considered a primary vector for F. tularensis, Amblyomma americanum is the most abundant tick species in this endemic region. A systematic study of F. tularensis colonization of A. americanum was undertaken to better understand its potential to serve as an overwintering reservoir for F. tularensis and as a bridging vector for human infections. Colony-reared A. americanum were artificially fed F. tularensis subspecies holarctica strain LVS via glass capillaries and colonization levels determined. Capillary-fed larva and nymph were initially infected with 104 CFU/tick which declined prior to molting for both stages, but rebounded post-molting in nymphs and persisted in 53% at 103 to 108 CFU/nymph at 168 days post-capillary feeding (longest sampling time in the study). In contrast, only 18% of adults molted from colonized nymphs maintained LVS colonization at 101 to 105 CFU/adult at 168 days post-capillary feeding (longest sampling time). For adults, LVS initially colonized the gut and disseminated to salivary glands by 24 h and had an ID50 of <5CFU in mice. Francisella tularensis infected the ovaries of gravid females, but transmission to eggs was infrequent and transovarial transmission to hatched larvae was not observed. The prolonged persistence of F. tularensis in A. americanum nymphs supports A. americanum as an overwintering reservoir for F. tularensis from which seasonal epizootics may originate; however, although the rapid dissemination of F. tularensis from gut to salivary glands in adults A. americanum is compatible with intermittent feeding adult males acting as bridging vectors for incidental F. tularensis infections of humans, acquisition of F. tularensis by adults may be unlikely based on adult feeding preference for larger mammals which are not involved in maintenance of sylvatic tularemia.

Highlights

  • The γ-proteobacterium Francisella tularensis subspecies tularensis can cause severe systemic infections in natural rabbit hosts and incidental infections in humans in its endemic region in the south-central United States [1,2,3]

  • We found that A. americanum nymphs which acquired F. tularensis colonization as larvae are able to maintain colonization for sufficient duration and at sufficient quanta to potentially maintain F. tularensis in the endemic region from one season to the ; the feeding preference of A. americanum nymphs and adults for larger mammals may reduce its importance for maintenance of the tularemia enzootic cycle in rabbits but may facilitate its role as a bridging vector for tularemia in humans

  • To assess quanta and duration of infection in larval A. americanum and transstadial transmission of F. tularensis to nymphs molted from infected larvae, larvae fed to repletion on rabbits were exposed to LVS by capillary feeding tick meal containing 107 CFU/mL LVS

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Summary

Introduction

The γ-proteobacterium Francisella tularensis subspecies tularensis can cause severe systemic infections in natural rabbit hosts and incidental infections in humans in its endemic region in the south-central United States [1,2,3] In this endemic region, tularemia is primarily a tick-vectored disease with a spring-summer seasonal pattern corresponding to the questing period of its tick vectors [1]. The distribution of F. tularensis in tick tissues of nymph and adults was determined as well as examination of transovarial transmission and transmission to rodents via tick saliva These studies were accomplished using an artificial colonization method of feeding F. tularensis to various tick stages using glass capillary tubes placed over the tick mouthparts

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