Tick-borne pathogen detection in midgut and salivary glands of adult Ixodes ricinus

Lejal et al. Parasites Vectors (2019) 12:152
https://doi.org/10.1186/s13071-019-3418-7

Abstract

Background:

The tick midgut and salivary glands represent the primary organs for pathogen acquisition and trans‑
mission, respectively. Specifcally, the midgut is the frst organ to have contact with pathogens during the blood meal
uptake, while salivary glands along with their secretions play a crucial role in pathogen transmission to the host. Cur‑
rently there is little data about pathogen composition and prevalence in Ixodes ricinus midgut and salivary glands. The
present study investigated the presence of 32 pathogen species in the midgut and salivary glands of unfed I. ricinus
males and females using high-throughput microfuidic real-time PCR. Such an approach is important for enriching the
knowledge about pathogen distribution in distinct tick organs which should lead to a better understanding I. ricinusborne disease epidemiology.

Results:

Borrelia lusitaniae, Borrelia spielmanii and Borrelia garinii, were detected in both midgut and salivary glands
suggesting that the migration of these pathogens between these two organs might not be triggered by the blood
meal. In contrast, Borrelia afzelii was detected only in the tick midgut. Anaplasma phagocytophilum and Rickettsia
helvetica were the most frequently detected in ticks and were found in both males and females in the midgut and
salivary glands. In contrast, Rickettsia felis was only detected in salivary glands. Finally, Borrelia miyamotoi and Babesia
venatorum were detected only in males in both midguts and salivary glands. Among all collected ticks, between
10–21% of organs were co-infected. The most common bacterial co-infections in male and female midgut and
salivary glands were Rickettsia helvetica+Anaplasma phagocytophilum and Rickettsia helvetica+Borrelia lusitaniae,
respectively.

Conclusions:

Analysing tick-borne pathogen (TBP) presence in specifc tick organs enabled us to (i) highlight
contrasting results with well-established transmission mechanism postulates; (ii) venture new hypotheses concern‑
ing pathogen location and migration from midgut to salivary glands; and (iii) suggest other potential associations
between pathogens not previously detected at the scale of the whole tick. This work highlights the importance
of considering all tick scales (i.e. whole ticks vs organs) to study TBP ecology and represents another step towards
improved understanding of TBP transmission.

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