The American Dog Tick, Dermacentor variabilis, as a Host of Bacterium tularense

Philip, Cornelius B.; Jellison, William L.

doi:10.2307/4581119

Cited by 31 publications

(25 citation statements)

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“…To date, we have found no evidence that white-footed mice are involved in the enzootic cycle. Because we were able to detect infection in host-seeking (i.e., nonfed) adult dog ticks, these ticks must have acquired infection either during their previous blood meals (transstadial transmission) or by inheritance (transovarial transmission [TOT] (32). Unfortunately, we were unable to assess the efficiency of TOT in our ticks, as none of the infected females collected from animals had fed long enough to lay eggs.…”

Section: Discussionmentioning

confidence: 93%

Genotypic Diversity of Francisella tularensis Infecting Dermacentor variabilis Ticks on Martha's Vineyard, Massachusetts

2004

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Martha's Vineyard, Mass., has been the site of two outbreaks of tularemia (1978 and 2000). Although most patients from both outbreaks presented with pneumonic disease and although aerosol transmission has been suggested, the bite of a dog tick and exposure to rabbits remain the only proven modes of transmission. The factors that precipitated the tularemia outbreaks or the proximal determinants of human risk remain undescribed. We sought to test the hypothesis that the ongoing outbreak is due to a recent introduction event as opposed to amplification of a cryptic enzootic cycle. From 2001-2003, we collected 4,246 dog ticks and tested them in pools for evidence of tularemia by PCR. We then measured the genetic diversity of Francisella tularensis by using multiple-locus variable-number tandem repeat analysis. The prevalence of F. tularensis in dog ticks averaged 0.7%. From 29 positive pools, we identified 10 unique genotypes, which was an unexpectedly large degree of diversity (Simpson's index ‫؍‬ 0.86). This degree of genetic diversity is inconsistent with a recent introduction event. We conclude that there has been long-standing enzootic transmission of tularemia on the island.

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Section: Discussionmentioning

confidence: 93%

Genotypic Diversity of Francisella tularensis Infecting Dermacentor variabilis Ticks on Martha's Vineyard, Massachusetts

2004

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“…The highest incidence of F. tularensis human infections and D. variabilis habitat overlap in geographic distribution (9,11,12). F. tularensis has been identified in adult D. variabilis ticks collected from the environment (11).…”

mentioning

confidence: 99%

Reproducible and Quantitative Model of Infection of Dermacentor variabilis with the Live Vaccine Strain of Francisella tularensis

Coburn

Maier

Casey

et al. 2015

Appl Environ Microbiol

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Pathogen life cycles in mammalian hosts have been studied extensively, but studies with arthropod vectors represent considerable challenges. In part this is due to the difficulty of delivering a reproducible dose of bacteria to follow arthropod-associated replication. We have established reproducible techniques to introduce known numbers of Francisella tularensis strain LVS from mice into Dermacentor variabilis nymphs. Using this model infection system, we performed dose-response infection experiments and followed bacterial replication through the molt to adults and at later time points. During development to adults, bacteria replicate to high numbers and can be found associated with the gut tissues, salivary glands, and hemolymph of adult ticks. Further, we can transmit a mutant of LVS (LVS ⌬purMCD) that cannot replicate in macrophages in vitro or in mice to nymphs. Our data show that the LVS ⌬purMCD mutant cannot be transstadially transmitted from nymphs to adult ticks. We then show that a plasmid-complemented strain of this mutant is recoverable in adult ticks and necessary for bacterial replication during the molt. In a mixed-infection assay (⌬purMCD mutant versus ⌬purMCD complement), 98% of the recovered bacteria retained the plasmid marker. These data suggest that the ⌬purMCD mutation cannot be rescued by the presence a complemented strain in a mixed infection. Importantly, our infection model provides a platform to test specific mutants for their replication in ticks, perform competition studies, and use other genetic techniques to identify F. tularensis genes that are expressed or required in this unique environment.F rancisella tularensis, a highly infectious zoonotic pathogen, causes a variety of syndromes collectively known as tularemia (1). Transmission of the organism to humans occurs by several routes, including contact with infected animal tissues, ingestion of contaminated food or water, exposure to biting flies, mosquitos, and ticks, or through aerosols (1-5). In the United States, acquisition of the bacterium is most often mediated by contact with infected rabbits or through the bite of an infected tick (6, 7). Since small mammals succumb to F. tularensis infection rapidly, a critical reservoir for maintenance of the organism in enzootic infection is the tick (8).The American dog tick, Dermacentor variabilis, appears to play a major role as a bridging vector to humans (9, 10). The highest incidence of F. tularensis human infections and D. variabilis habitat overlap in geographic distribution (9,11,12). F. tularensis has been identified in adult D. variabilis ticks collected from the environment (11). Moreover, experimental work has shown that type A (A1a, A1b, and A2) as well as virulent type B strains of F. tularensis can be transmitted from infected mice to larval ticks and that these ticks develop to the nymphal stage and can transmit the infection to naive animals (9). Transmission was, however, inefficient, as the bacterial infection affected tick fitness and mortality (9). In more recent ...

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“…A seminal study of tick competence for F. tularensis (Philip and Jellison 1934) as well as a recent study (Reese et al 2010) demonstrated that infected ticks die, similar to the effects on fitness seen for Rickettsia rickettsii in wood ticks (Niebylski et al 1999). The degree to which ticks serve as long-term reservoirs would depend on the prevalence and intensity of a negative fitness effect.…”

Section: Vector-borne and Zoonotic Diseasesmentioning

confidence: 81%

Differential Mortality of Dog Tick Vectors Due to Infection by DiverseFrancisella tularensis tularensisGenotypes

Goethert

Telford

2011

Vector-Borne and Zoonotic Diseases

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The factors involved in the long-term perpetuation of Francisella tularensis tularensis in nature are poorly understood. Martha's Vineyard, Massachusetts, has become a site of sustained transmission of Type A tularemia, with nearly 100 human cases reported from 2000 to 2010. We have identified a stable focus of F. tularensis transmission there, where the annual prevalence in host-seeking Dermacentor variabilis is about 3%, suggesting that this tick perpetuates the agent. However, laboratory studies have shown that infection with F. tularensis has a profound negative effect on dog tick mortality, presenting a paradox: how can a vector perpetuate an agent that negatively affects its fitness? It may be that experimental infection does not mimic that of natural transmission. Accordingly, we examined the effects that F. tularensis has on the longevity of field-derived ticks. Of 63 PCR-positive ticks collected in early summer, 89% were dead by December compared to 48% of 214 uninfected ticks collected at the same time and site. However, the quantum of F. tularensis DNA within each tick was not correlated with increased mortality. Instead, ticks with an uncommon genotype were more likely to die early than those with the common genotype. We conclude that the interaction between F. tularensis and its vector is complex and certain bacterial genotypes appear to be better adapted to their arthropod host.

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The American Dog Tick, Dermacentor variabilis, as a Host of Bacterium tularense

Cited by 31 publications

References 1 publication

Genotypic Diversity of Francisella tularensis Infecting Dermacentor variabilis Ticks on Martha's Vineyard, Massachusetts

Genotypic Diversity of Francisella tularensis Infecting Dermacentor variabilis Ticks on Martha's Vineyard, Massachusetts

Reproducible and Quantitative Model of Infection of Dermacentor variabilis with the Live Vaccine Strain of Francisella tularensis

Differential Mortality of Dog Tick Vectors Due to Infection by DiverseFrancisella tularensis tularensisGenotypes

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