Seasonal Prevalence of Lyme Disease Spirochetes in a Heterothermic Mammal, the Edible Dormouse (Glis glis)

Abstract

cIn Europe, dormice serve as competent reservoir hosts for particular genospecies of the tick-borne agent of Lyme disease (LD) and seem to support them more efficiently than do mice or voles. The longevity of edible dormice (Glis glis) and their attractiveness for ticks may result in a predominance of LD spirochetes in ticks questing in dormouse habitats. To investigate the role of edible dormice in the transmission cycle of LD spirochetes, we sampled skin tissue from the ear pinnae of dormice inhabiting five different study sites in south western Germany. Of 501 edible dormice, 12.6% harbored DNA of LD spirochetes. Edible dormice were infected most frequently with the pathogenic LD spirochete Borrelia afzelii. The DNA of B. garinii and B. bavariensis was detected in ca. 0.5% of the examined individuals. No spirochetal DNA was detectable in the skin of edible dormice until July, 6 weeks after they generally start to emerge from their obligate hibernation. Thereafter, the prevalence of spirochetal DNA in edible dormice increased during the remaining period of their 4 to 5 months of activity, reaching nearly 40% in September. Males were more than four times more likely to harbor LD spirochetes than females, and yearlings were almost twice more likely to be infected than adults. The seasonality of the prevalence of LD spirochetes in edible dormice was pronounced and may affect their role as a reservoir host in respect to other hosts.

The vector tick Ixodes ricinus feeding on an arboreal rodent—the edible dormouse Glis glis

“…Considering that nymphal I. ricinus ticks feed for 4 to 5 days (Matuschka et al 1991) and that, on average, every eighth nymph harbors B. afzelii in this region Matuschka 2006, 2011), the 4 % edible dormice parasitized by a nymph at any one time in June may receive an spirochetal inoculation within the span of 4 to 5 weeks (4 × 8 = 32 days). Indeed, we detected 3.6 % spirochetal prevalence in edible dormice a month later, during July (Fietz et al 2014b). That the increase in prevalence is delayed by about a month in respect to the increase in nymphal infestation rates supports also the interpretation of our previous finding that the population of edible dormice is only incrementally infected after a complete loss of spirochetal infection during hibernation.…”

“…In a previous study, we observed that none of the 103 edible dormice captured during May and June contained spirochetal DNA and only very few did so in July, although prevalence of infection in these populations reached 40 % in September (Fietz et al 2014b). Considering that LD spirochetes generally disseminate in their rodent host in the course of about 2 weeks (Richter et al 2002, the observed delay in prevalence may derive from either of three reasons: (a) edible dormice are not susceptible to tick-borne spirochetes at their emergence from hibernation and become more susceptible throughout the season, (b) spirochetal dissemination in edible dormice is somehow delayed compared with other rodents, or (c) the likelihood of edible dormice to encounter infected nymphal ticks increases during the course of the season.…”

“…Our observations that half the females, as compared with males, were infested by nymphs in August when raising their young and that infestation rates equaled in September suggests a causal relationship between forage activity of dormice and nymphal infestation rates. Similarly, male dormice are several times more likely to harbor LD spirochetes than females throughout the season of activity, but most pronounced during August (Fietz et al 2014b). Sex-specific behavioral differences appear to increase the likelihood of males to encounter infected nymphs and consequently to acquire tick-borne LD spirochetes; as a result, males would appear to contribute more efficiently to the transmission cycle than females.…”

“…In nature, edible dormice most frequently harbor the pathogenic LD spirochete Borrelia afzelii (Fietz et al 2014b). During their obligate hibernation, edible dormice appear to lose their spirochetal infection (Fietz et al 2014b).…”

“…During their obligate hibernation, edible dormice appear to lose their spirochetal infection (Fietz et al 2014b). And reinfection seemed delayed, as no spirochetal DNA was detectable in any individuals captured before July, although dormice emerge from hibernation about 6 weeks earlier.…”