Larvae of Ixodes ricinus transmit Borrelia afzelii and B. miyamotoi to vertebrate hosts

Abstract

BackgroundLyme borreliosis is the most common tick-borne human disease and is caused by Borrelia burgdorferi sensu lato (s.l.). Borrelia miyamotoi, a relapsing fever spirochaete, is transmitted transovarially, whereas this has not been shown for B. burgdorferi (s.l). Therefore, B. burgdorferi (s.l) is considered to cycle from nymphs to larvae through vertebrates. Larvae of Ixodes ricinus are occasionally B. burgdorferi (s.l) infected, but their vector competence has never been studied.MethodsWe challenged 20 laboratory mice with field-collected larvae of I. ricinus. A subset of these larvae was analysed for infections with B. burgdorferi (s.l) and B. miyamotoi. After three to four challenges, mice were sacrificed and skin and spleen samples were analysed for infection by PCR and culture.ResultsField-collected larvae were naturally infected with B. burgdorferi (s.l) (0.62 %) and B. miyamotoi (2.0 %). Two mice acquired a B. afzelii infection and four mice acquired a B. miyamotoi infection during the larval challenges.ConclusionWe showed that larvae of I. ricinus transmit B. afzelii and B. miyamotoi to rodents and calculated that rodents have a considerable chance of acquiring infections from larvae compared to nymphs. As a result, B. afzelii can cycle between larvae through rodents. Our findings further imply that larval bites on humans, which easily go unnoticed, can cause Lyme borreliosis and Borrelia miyamotoi disease.

Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks

“…It has been shown previously that ixodid ticks are able to complete feeding on a second host after interruption (29); thus, partially fed ticks may be sampled as seemingly unfed larvae. This finding, together with the recent findings that I. ricinus larvae are able to transmit B. afzelii to laboratory mice (30), suggests the potential role of larvae in spreading human LB (30).…”

Do Tick Attachment Times Vary between Different Tick-Pathogen Systems?

“…ticks sampled [67] and 0.7-1.7% of I. pacificus ticks tested in California [68]. It has been found in~12% of ticks tested in parts of Indiana [66] and transovarial transmission has been shown in I. scapularis [52] and I. ricinus [69]. The first cases of B. miyamotoi-infected humans were reported in Russia in 2011 [70,71].…”

The wild life of tick-borne pathogens

“…This could be either due to a high host density Borrelia miyamotoi Bank vole, Wood mouse (Rodents) and trans-ovarial transmission 50,256 or a high activity level of host individuals. Therefore, we used the number of animals walking past a location in the plot per day, measured as their passage rate, as a measure of host availability to ticks.…”

“…This assumption only holds for certain pathogens that are not trans-ovarially transmitted 22 and for host species that do not feed adult ticks. However, even pathogens that are considered not to be trans-ovarially transmitted, such as B. afzelii, can still be found in very low prevalence in questing larvae, which can therefore have a major contribution to infection in rodents 256 . Incorporating infection by larvae into the model would further increase the importance of daily distance travelled as an important determinant of infection prevalence in hosts and subsequently in infected nymphs.…”