Tick-Borne Encephalitis Virus Transmission between Ticks Cofeeding on Specific Immune Natural Rodent Hosts

Abstract

To determine whether the portion of a vertebrate host population having specific immunity to tick-borne encephalitis (TBE) virus can participate in the TBE virus transmission cycle, natural hosts immunized against TBE virus were challenged with infected and uninfected ticks. Yellow-necked field mice (Apodemus flavicollis) and bank voles (Clethrionomys glareolus) were either immunized with TBE virus by subcutaneous inoculation of the virus, or they were exposed to virus-infected Ixodes ricinus ticks. One month later, when serum neutralizing antibody was detectable, the animals were infested with infected (donor) adult female ticks and uninfected (recipient) nymphal ticks; recipients were allowed to feed either in close contact (chamber 1) or physically separated (chamber 2) from the infected donor ticks. Following challenge with infected (and uninfected) ticks, viremia developed in all the control, nonimmune animals, whereas viremia was undetectable in all those animals naturally immunized by previous exposure to infected ticks. Despite the presence of neutralizing antibodies in all the immunized animals, 89% (24/ 27) immune animals supported virus transmission between infected and uninfected cofeeding ticks. Most transmission was localized, occurring within chamber 1; disseminated transmission from chamber 1 to chamber 2 was reduced. Immunization by tick bite was more effective than immunization by syringe inoculation in blocking cofeeding virus transmission. Nevertheless 76% (9/12) animals with "natural" immunity still supported transmission. The results demonstrate that natural hosts having neutralizing antibodies to TBE virus (and no detectable viremia) can still support virus transmission between infected and uninfected ticks feeding closely together on the same animal. These observations have important epidemiological implications relating to the survival of TBE virus in Nature.

Empirical evidence for key hosts in persistence of a tick-borne disease

“…TBE endemic cycles in A. flavicollis are maintained via the co-feeding process (Labuda et al, 1997). Therefore we investigated the characteristics of hosts with co-feeding, by use of a GLMM via an IRREML procedure (Genstat 4.2, 5th Edition) with binomial errors and co-feeding presence as the response variate.…”

“…We examined transmission patterns through a capturemark-recapture (CMR) study of the yellow-necked mouse, Apodemus flavicollis, and their associated infestations with the sheep tick, Ixodes ricinus, the vector of the zoonotic disease tick-borne encephalitis (TBE) (Labuda et al, 1997). This disease is second only to Lyme disease as the most important vector-borne zoonotic disease in Europe with 10,000 human cases per annum reported from mainland Europe (http://www.tbe-info.com).…”

“…TBE virus is transmitted to susceptible ticks when they feed adjacent to infected ticks, through a process known as co-feeding which does not involve virus amplification within the host (Jones et al, 1987;Labuda et al, 1993). Transmission is facilitated by tick saliva and occurs only on specific hosts, for example, A. flavicollis (Labuda et al, 1997) and depends on cellular events such as invasion of immune cells that are transported to the lymph nodes. In the absence of co-feeding and suitable nonviraemic hosts, the threshold for disease persistence (measured by the reproductive number, R 0 ), falls below unity and TBE fades out (Randolph et al, 1996).…”

High-Throughput Procedure for Tick Surveys of Tick-Borne Encephalitis Virus and Its Application in a National Surveillance Study in Switzerland

“…Ticks are infected chronically throughout their life cycle (17). In addition to this transstadial transmission, the virus is spread transovarially (6) or between ticks feeding on the same host (21). As they are more numerous than adults, nymphs are thought to be the most important stage in the transmission of the virus (39).…”

Critical Contact Rate for Vector–host–pathogen Oscillation Involving Co-Feeding and Diapause

“…Whether co-feeding transmission takes place or not depends on a large number of factors including the co-feeding duration and the density and (physical) proximity of A-stage infected ticks to the susceptible B-stage ticks. 10,11 Here, we made a simplified assumption that there are only two groups of hosts: those in which co-feeding can take place and those co-feeding cannot happen (note that this is different from the assumption whether the host has one or none infested tick). A more realistic model formulation will have to involve the density and spatial distributions of the infected A-stage ticks and their relative spatial locations to the B-stage susceptible ticks within the same host.…”