Most of the data on oral infections of ticks with tick-borne encephalitis virus have been derived from experiments using animals infected by syringe inoculation. To mimic the natural conditions of virus transmission, tick-borne encephalitis virus-infected Ixodes ricinus (Linnaeus) or Rhipicephalus appendiculatus Neumann adults (donors) were cofed with uninfected nymphs (recipients) of either tick species on uninfected guinea pigs. Two tick-retaining cells were attached to each guinea pig: cell 1 contained uninfected nymphs and virus-infected adults, and cell 2 contained uninfected nymphs. Following engorgement, 55% of I. ricinus nymphs and 65% of R. appendiculatus nymphs were shown to have acquired the virus while cofeeding with I. ricinus donor ticks. Similarly, 66% of R. appendiculatus recipient nymphs that cofed with R. appendiculatus virus-infected adults were infected. Some of the guinea pigs on which the ticks cofed were apparently nonviremic. The results indicate that efficient transmission of tick-borne encephalitis virus can occur between cofeeding ticks even when the host on which they feed does not develop a detectable viremia.
In nature, infected and uninfected arthropod vectors often feed together on an animal. In mimicking this scenario in the laboratory, uninfected vectors were found to acquire virus while cofeeding on the same host as infected vectors. However, the vertebrate host on which they fed did not develop detectable levels of virus in its blood. These observations were made with Thogoto virus, an influenza-like virus of medical and veterinary significance. Rhipicephalus appendiculatus ticks were used as the vector and guinea pigs as the vertebrate host. The results demonstrate that a vertebrate that is apparently refractory to infection by an arthropod-borne virus can still play an important role in the epidemiology of the virus, and they suggest a novel mode of arthropod-borne virus transmission.
To investigate the role of ticks in TBE virus transmission, salivary gland extract (SGE) was derived from partially fed female Ixodes ricinus, Dermacentor reticulatus and Rhipicephalus appendiculatus ticks. Guinea-pigs were infested with uninfected R. appendiculatus nymphs and inoculated with a mixture of TBE virus and SGE or with virus alone. The number of ticks which on average acquired virus from feeding on animals inoculated with TBE virus and SGE from partially fed ticks was 4-fold greater than the number that became infected by feeding on animals inoculated with virus alone or virus plus SGE from unfed I. ricinus. Viraemia was detected in 67% of guinea-pigs inoculated with virus plus SGE compared to 30% of guinea-pigs inoculated with virus alone. Virus titres in the blood were similar for both groups of animals [range 2.0-2.8 log10 plaque-forming units (PFU)/ml of blood]; however, the number of ticks that became infected was significantly higher on animals inoculated with virus plus SGE from partially fed ticks. No significant difference was observed with respect to the tick species used to derive SGE. The results indicate that TBE virus transmission is enhanced by factor(s) associated with the salivary glands of feeding ticks, and that these factor(s) may facilitate efficient transmission of TBE virus between infected and uninfected ticks even when they feed on hosts that have no detectable viraemia.
Most of the data on oral infection of ticks by louping ill virus have been obtained from experiments in which animals were infected by syringe inoculation with infectious material. Using infected ticks to mimic the natural situation, we have demonstrated that louping ill (LI) virus transmission can occur from infected to uninfected Ixodes ricinus feeding in close proximity on mountain hares (Lepus timidus). Under these conditions the hares developed either low or undetectable viraemias. Highest prevalence of LI virus infection was observed in recipient nymphs which had fed to repletion between days 3 and 7 post-attachment of virus-infected adults; following engorgement, 56% of nymphs acquired virus. These results demonstrate the efficient transmission of LI virus between co-feeding ticks on naive mountain hares. However, when ticks were allowed to co-feed on virus-immune hares a significant reduction in the frequency of infection was observed. Neither red deer (Cervus elaphus) nor New Zealand White rabbits supported transmission of LI virus. The significance of virus transmission between cofeeding ticks on LI virus epidemiology is discussed.
1895 SUMMARYPrevious studies have demonstrated that Thogoto (THO) virus is transmitted from infected to uninfected ticks cofeeding on an uninfected guinea-pig, although the guinea-pig does not develop a detectable viraemia. To investigate this mode of transmission, guinea-pigs were infested with uninfected Rhipicephalus appendiculatus nymphs prior to inoculation with either a mixture of THO virus and tick salivary gland extract, or with THO virus alone. The number of ticks that acquired the virus from feeding on animals inoculated with a mixture of virus and salivary gland extract was 10-fold greater than the number that became infected by feeding on animals inoculated with virus alone. The increase in the number of ticks that became infected was greatest when the salivary glands used in the inoculum were derived from uninfected ticks, which had partially fed for a period of 6 days. Viraemia was not detected in any of the guinea-pigs tested during the experiments. These results indicate that THO virus transmission is enhanced by factor(s) associated with the salivary glands of ticks, and that these factor(s) may facilitate 'non-viraemic' transmission between infected and uninfected ticks.In nature, infected and uninfected vectors of arthropod-transmitted viruses must frequently feed together on the same vertebrate host. In general, the host is considered to take part in the virus transmission cycle if it becomes infected and develops viraemia, providing a virus-laden blood-meal for the vector. On this premise, animals are considered important in the epidemiology of an arthropod-borne virus disease if they develop a viraemia that satisfies the threshold level considered necessary to infect the arthropod vector (Hardy et al., 1983). However, in the laboratory we have demonstrated that transmission of a tick-borne virus can occur without the vertebrate developing a detectable viraemia. Moreover, in these studies 'nonviraemic transmission' (NVT) was more efficient than classical 'viraemic transmission' (Jones et al., 1987). This study was undertaken to investigate the mechanism of NVT.Experiments were conducted with Thogoto (THO) virus, a virus of medical and veterinary significance that is structurally and morphogenetically similar to the influenza viruses (Haig et al., 1965;Clerx et al., 1983;Davies et al., 1986). The virus was originally isolated from ticks collected in Kenya (Haig et al., 1965) and has subsequently been detected throughout central Africa and in parts of the Middle East and southern Europe (Davies et al., 1986).THO virus is transmitted biologically by the African three-host ixodid tick species, Rhipicephalus appendiculatus (Davies et al., 1986). A laboratory colony of R, appendiculatus was maintained by feeding the ticks on guinea-pigs as previously described (Jones et al., 1988). The inter-feeding stages were maintained in perforated tubes held inside a desiccator at a temperature of 28 °C and at 809/oo relative humidity. The Sicilian SiAr isolate of THO virus (Albanese et al., 1972) was used t...
Arboviruses differ from other viruses in their need to replicate in both vertebrate and invertebrate hosts. The invertebrate is a blood-sucking arthropod that is competent to transmit the virus between susceptible animals. Arboviruses transmitted by ticks must adapt to the peculiar physiological and behavioral characteristics of ticks, particularly with regard to blood feeding, bloodmeal digestion, and molting. Virus imbibed with the blood meal first infects cells of the midgut wall. During this phase the virus must contend with the heterophagic bloodmeal digestion of ticks (an intracellular process occurring within midgut cells) and overcome the as yet undefined "gut barrier" to infection. Genetic and molecular data for a number of tick-borne viruses indicate ways in which such viruses may have adapted to infecting ticks, but far more information is needed. After infection of midgut cells, tick-borne viruses pass to the salivary glands for transmission during the next blood-feeding episode. To do this, the virus must survive molting by establishing an infection in at least one cell type that does not undergo histolysis. Different tick-borne viruses have different strategies for surviving the molting period, targeting a variety of tick tissues. The infection can then persist for the life span of the tick with little evidence of any detrimental effects on the tick. Transmission to a vertebrate host during feeding most probably occurs via saliva that contains virus secreted from infected salivary gland cells. The virus then enters the skin site of feeding, which has been profoundly modified by the pharmacological effects of tick saliva. At least three tick-borne viruses exploit such tick-induced host changes. This phenomenon (saliva-activated transmission) is believed to underlie "nonviremic transmission," whereby a virus is transmitted from an infected to an uninfected cofeeding tick through a host that has an undetectable or very low viremia. Thus tick-borne viruses that have adapted to the feeding characteristics of their tick vectors may not need to induce a virulent infection (with high viremia) in their natural vertebrate hosts. Efficient transmission of tick-borne viruses between cofeeding ticks may be a means of amplifying virus infection prevalence in F1 generations infected by transovarial transmission.
Ixodes ricinus ticks were collected from dragging vegetation and from shot roe deer in the province of Trento and Belluno in northern Italy. Ticks were pooled for analyses and from 1060 pools of ticks collected in the province of Belluno and 12390 tick samples collected in Trentino, four proved positive by immunofluorescence microscopy using a tick-borne encephalitis (TBE)-specific antiserum. The identity of the virus isolates was determined by RT-PCR cycle sequencing and they were all found to be closely similar (> 98% nucleotide identity) to typical western European TBE complex viruses as found in Austria. The isolates from Trentino differed from the Neudorfl strain of western European TBE virus at eight nucleotide positions but as these nucleotide substitutions were all synonymous, there were no amino acid changes. These results imply that the virus isolates in Trentino have changed slightly from the typical European strains isolated in nearby Austria. The abundance of questing ticks and ticks feeding on roe deer was greater in TBE positive hunting districts than in hunting districts where TBE complex viruses were only probable or believed to be absent. In TBE positive and probable districts synchrony in the seasonal dynamics of larvae and nymphs of L. ricinus was observed. This study provides evidence to suggest that roe deer may have an important role to play in the maintenance of tick density and in the persistence of TBE virus.
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