Importance of Localized Skin Infection in Tick-Borne Encephalitis Virus Transmission

Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia.
Virology (Impact Factor: 3.32). 06/1996; 219(2):357-66. DOI: 10.1006/viro.1996.0261
Source: PubMed


Arboviruses are transmitted to vertebrates by the "bite" of infected arthropods. Events at the site of virus deposition are largely unknown despite increasing evidence that blood-sucking arthropods immunomodulate their skin site of feeding. This question is particularly relevant for ixodid ticks that feed for several days. To examine events under conditions mimicking tick-borne encephalitis (TBE) virus transmission in nature (i.e., infected and uninfected Ixodes ricinus ticks feeding on the same animal), infected adult and uninfected nymphal ticks were placed in one retaining chamber (skin site A) and uninfected nymphs were placed within a second chamber posteriorly (skin site B) on two natural host species, yellow-necked field mice (Apodemus flavicollis) and bank voles (Clethrionomys glareolus). Virus transmission from infected to uninfected cofeeding ticks was correlated with infection in the skin site of tick feeding. Furthermore, virus was recruited preferentially to the site in which ticks were feeding compared with uninfested skin sites. Viremia did not correspond with a generalized infection of the skin; virus was not detected in an uninfested skin site (C) of 12/13 natural hosts that had viremia levels > or = 2.0 log10 ic mouse LD50/0.02 ml blood. To characterize infected cells, laboratory mouse strains were infested with infected ticks and then explants were removed from selected skin sites and floated on culture medium. Numerous leukocytes were found to migrate from the skin explants of tick feeding sites. Two-color immunocytochemistry revealed viral antigen in both migratory Langerhans cells and neutrophils; in addition, the migratory monocyte/macrophages were shown to produce infectious virus. The results indicate that the local skin site of tick feeding is an important focus of viral replication early after TBE virus transmission by ticks. Cellular infiltration of tick feeding sites, and the migration of cells from such sites, may provide a vehicle for transmission between infected and uninfected cofeeding ticks that is independent of a patent viremia. The data support the hypothesis that viremia is a product, rather than a prerequisite, of tick-borne virus transmission.

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    • "However, after 3 days of co-feeding, infectious virus was detected only in their bodies and not in their SG. In previous studies aimed to understand the role of local skin infection and saliva assisted transmission in non-viraemic co-feeding transmission, the percentage of I. ricinus nymphs acquiring TBEV increased in parallel with the duration of co-feeding on natural rodent hosts as well as on laboratory mice from day 1 to day 3 (Labuda et al., 1996). Similar results were achieved by infestation of yellow-necked mice with infected I. ricinus females and short-feeding Haemaphysalis inermis nymphs (Labuda et al., unpublished). "
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    ABSTRACT: Biotic factors contributing to the survival of tick-borne viruses in nature are poorly understood. Using tick-borne encephalitis virus (TBEV) and its principal European vector, Ixodes ricinus, we examined the relative roles of salivary gland infection, co-feeding transmission, and moulting in virus survival. Virus titres in the salivary glands increased after blood-feeding in a time- and dose-dependent manner. This was observed in ticks infected by inoculation but not in ticks infected by the natural route of co-feeding. Amplification of infection prevalence occurred via co-feeding. However, when larvae or nymphs subsequently moulted, the infection prevalence dramatically declined although this was not observed when ticks were infected by inoculation. Trans-stadial survival is a hitherto overlooked parameter that may contribute to the low incidence of TBEV infection in field-collected I. ricinus ticks.
    Full-text · Article · Oct 2014 · Ticks and Tick-borne Diseases
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    • "Co-feeding transmission of TBEV appears to be mediated by migratory leucocytes . Langerhans cells, the dendritic cells that reside in the skin, appear to be recruited to the tick-feeding site where they acquire TBEV (Labuda et al. 1996). Infected Langerhans cells are believed to transmit the virus to T lymphocytes in the local lymph nodes (Nuttall, 1999; Nuttall and Labuda, 2003). "
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    ABSTRACT: This review examines the phenomenon of co-feeding transmission in tick-borne pathogens. This mode of transmission is critical for the epidemiology of several tick-borne viruses but its importance for Borrelia burgdorferi sensu lato, the causative agents of Lyme borreliosis, is still controversial. The molecular mechanisms and ecological factors that facilitate co-feeding transmission are therefore examined with particular emphasis on Borrelia pathogens. Comparison of climate, tick ecology and experimental infection work suggests that co-feeding transmission is more important in European than North American systems of Lyme borreliosis, which potentially explains why this topic has gained more traction in the former continent than the latter. While new theory shows that co-feeding transmission makes a modest contribution to Borrelia ␣tness, recent experimental work has revealed new ecological contexts where natural selection might favour co-feeding transmission. In particular, co-feeding transmission might confer a ␣tness advantage in the Darwinian competition among strains in mixed infections. Future studies should investigate the ecological conditions that favour the evolution of this fascinating mode of transmission in tick-borne pathogens.
    Full-text · Article · Aug 2014 · Parasitology
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    • "Small mammals play a central role in virus transmission between ticks and are important hosts in tick life cycle. As non-viremic host, they are essential for transmission of TBEV by co-feeding of infected and non-infected ticks [20], [21], [22], [23]. Additionally, viremia in small mammals is sufficiently high and most likely not as short termed as previously thought to enable direct transmission of the virus to feeding ticks [24], [25], [26], [27]. "
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    ABSTRACT: Tick-borne encephalitis (TBE) is a virus infection which sometimes causes human disease. The TBE virus is found in ticks and certain vertebrate tick hosts in restricted endemic localities termed TBE foci. The formation of natural foci is a combination of several factors: the vectors, a suitable and numerous enough number of hosts and in a habitat with suitable vegetation and climate. The present study investigated the influence of deer on the incidence of tick-borne encephalitis. We were able to obtain data from deer culls. Using this data, the abundance of deer was estimated and temporal and spatial analysis was performed. The abundance of deer has increased in the past decades, as well as the incidence of tick-borne encephalitis. Temporal analysis confirmed a correlation between red deer abundance and tick-borne encephalitis occurrence. Additionally, spatial analysis established, that in areas with high incidence of tick-borne encephalitis red deer density is higher, compared to areas with no or few human cases of tick-borne encephalitis. However, such correlation could not be confirmed between roe deer density and the incidence of tick-borne encephalitis. This is presumably due to roe deer density being above a certain threshold so that availability of tick reproduction hosts has no apparent effect on ticks' host finding and consequently may not be possible to correlate with incidence of human TBE.
    Full-text · Article · Jun 2013 · PLoS ONE
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