Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.

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...

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Main Authors: Rinosh J Mani, Jessica Abbey Metcalf, Kenneth D Clinkenbeard
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0130513
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spelling doaj-0347afa6959943cda2b23026954df84b2021-03-03T20:01:13ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01106e013051310.1371/journal.pone.0130513Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.Rinosh J ManiJessica Abbey MetcalfKenneth D ClinkenbeardThe 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 10(4) CFU/tick which declined prior to molting for both stages, but rebounded post-molting in nymphs and persisted in 53% at 10(3) to 10(8) 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 10(1) to 10(5) 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.https://doi.org/10.1371/journal.pone.0130513
collection DOAJ
language English
format Article
sources DOAJ
author Rinosh J Mani
Jessica Abbey Metcalf
Kenneth D Clinkenbeard
spellingShingle Rinosh J Mani
Jessica Abbey Metcalf
Kenneth D Clinkenbeard
Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
PLoS ONE
author_facet Rinosh J Mani
Jessica Abbey Metcalf
Kenneth D Clinkenbeard
author_sort Rinosh J Mani
title Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
title_short Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
title_full Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
title_fullStr Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
title_full_unstemmed Amblyomma americanum as a Bridging Vector for Human Infection with Francisella tularensis.
title_sort amblyomma americanum as a bridging vector for human infection with francisella tularensis.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description 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 10(4) CFU/tick which declined prior to molting for both stages, but rebounded post-molting in nymphs and persisted in 53% at 10(3) to 10(8) 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 10(1) to 10(5) 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.
url https://doi.org/10.1371/journal.pone.0130513
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