Potential drivers of vector-borne pathogens in urban environments: European hedgehogs (Erinaceus europaeus) in the spotlight

Abstract

Vector-borne diseases (VBDs) are considered as (re-)emerging, but information on the transmission cycles and wildlife reservoirs is often incomplete, particularly with regard to urban areas. The present study investigated blood samples from European hedgehogs (Erinaceus europaeus) presented at wildlife rehabilitation centres in the region of Hanover. Past exposure to B. burgdorferi sensu lato (s.l.) and tick-borne encephalitis virus (TBEV) was assessed by serological detection of antibodies, while current infections with Borrelia spp., Anaplasma phagocytophilum, Rickettsia spp., Neoehrlichia mikurensis, Bartonella spp., Babesia spp. and Spiroplasma ixodetis were investigated by (q)PCR. Of 539 hedgehogs tested for anti-Borrelia antibodies, 84.8% (457/539) were seropositive, with a higher seropositivity rate in adult than subadult animals, while anti-TBEV antibodies were detected in one animal only (0.2%; 1/526). By qPCR, 31.2% (168/539) of hedgehog blood samples were positive for Borrelia spp., 49.7% (261/525) for A. phagocytophilum, 13.0% (68/525) for Bartonella spp., 8.2% for S. ixodetis (43/525), 8.0% (42/525) for Rickettsia spp. and 1.3% (7/525) for Babesia spp., while N. mikurensis was not detected. While further differentiation of Borrelia spp. infections was not successful, 63.2% of the A. phagocytophilum infections were assigned to the zoonotic ecotype I and among Rickettsia spp. infections, 50.0% to R. helvetica by ecotype- or species-specific qPCR, respectively. Sequencing revealed the presence of a Rickettsia sp. closely related to Rickettsia felis in addition to a Bartonella sp. previously described from hedgehogs, as well as Babesia microti and Babesia venatorum. These findings show that hedgehogs from rehabilitation centres are valuable sources to identify One Health pathogens in urban areas. The hedgehogs are not only exposed to pathogens from fleas and ticks in urban areas, but they also act as potent amplifiers for these vectors and their pathogens, relevant for citizens and their pets.

Keywords: Anaplasma phagocytophilum; Bartonella; Borrelia; Rickettsia; Tick-borne pathogens; Zoonoses.

Graphical abstract

Fig. 1

Overview of the study design investigating vector-borne pathogens in European hedgehogs from Northern Germany.

Fig. 2

Patterns of (a) B. burgdorferi s.l. ELISA results, (b) Borrelia spp. qPCR results and (c) A. phagocytophilum qPCR results in blood samples of European hedgehogs according to animal age class and over the course of the study. Sample sizes are indicated above the bars. Note that animals with undetermined age class were excluded from the panels on the left. No sampling was done in December 2020 and January 2021.

Fig. 3

Prevalence of (a) Rickettsia spp., (b) Bartonella spp., (c) Spiroplasma ixodetis and (d) Babesia spp. in blood samples of European hedgehogs according to animal age class and over the course of the study. Sample sizes are indicated above the bars of panel A and refer to all panels. Note that animals with undetermined age class were excluded from the panels on the left. No sampling was done in December 2020 and January 2021.

Supplementary Fig. S1

Amount of blood clot used for isolation of DNA from hedgehog blood samples (A) and Borrelia 5S-23S intergenic spacer (IGS) copies (B) in positive samples over the course of the study. Violin plots (C) illustrate the shape of the 5S-23S IGS copy number distribution in the different study years, with individual values shown as dots. The correlation between blood clot weight and 5S-23S IGS copy numbers is shown in panel D.