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Hedgehogs, Squirrels, and Blackbirds as Sentinel Hosts for Active Surveillance of Borrelia miyamotoi and Borrelia burgdorferi Complex in Urban and Rural Environments.

ABSTRACT: Lyme borreliosis (LB), caused by spirochetes of the Borrelia burgdorferi sensu lato (s.l.) complex, is one of the most common vector-borne zoonotic diseases in Europe. Knowledge about the enzootic circulation of Borrelia pathogens between ticks and their vertebrate hosts is epidemiologically important and enables assessment of the health risk for the human population. In our project, we focused on the following vertebrate species: European hedgehog (Erinaceus europaeus), Northern white-breasted hedgehog (E. roumanicus), Eurasian red squirrel (Sciurus vulgaris), and Common blackbird (Turdus merula). The cadavers of accidentally killed animals used in this study constitute an available source of biological material, and we have confirmed its potential for wide monitoring of B. burgdorferi s.l. presence and genospecies diversity in the urban environment. High infection rates (90% for E. erinaceus, 73% for E. roumanicus, 91% for S. vulgaris, and 68% for T. merula) were observed in all four target host species; mixed infections by several genospecies were detected on the level of individuals, as well as in particular tissue samples. These findings show the usefulness of multiple tissue sampling as tool for revealing the occurrence of several genospecies within one animal and the risk of missing particular B. burgdorferi s.l. genospecies when looking in one organ alone.

SUBMITTER: Majerova K

PROVIDER: S-EPMC7760222 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Hedgehogs, Squirrels, and Blackbirds as Sentinel Hosts for Active Surveillance of Borrelia miyamotoi and Borrelia burgdorferi Complex in Urban and Rural Environments.

Majerová Karolina K Hönig Václav V Houda Michal M Papežík Petr P Fonville Manoj M Sprong Hein H Rudenko Natalie N Golovchenko Maryna M Černá Bolfíková Barbora B Hulva Pavel P Růžek Daniel D Hofmannová Lada L Votýpka Jan J Modrý David D

Microorganisms 20201130 12

Lyme borreliosis (LB), caused by spirochetes of the Borrelia burgdorferi sensu lato (s.l.) complex, is one of the most common vector-borne zoonotic diseases in Europe. Knowledge about the enzootic circulation of Borrelia pathogens between ticks and their vertebrate hosts is epidemiologically important and enables assessment of the health risk for the human population. In our project, we focused on the following vertebrate species: European hedgehog (Erinaceus europaeus), Nor ...[more]

PMID: 33266311

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Project description:BackgroundBorrelia miyamotoi and Borrelia burgdorferi sensu lato (s.l.) are important zoonotic agents transmitted by Ixodes ricinus ticks, which are widely distributed across Central Europe. Understanding the spatial distribution of these pathogens' prevalence will help identify areas with increased infection risk and facilitate the implementation of effective preventive measures.MethodsWe analysed 12,955 I. ricinus ticks collected from 142 towns in the Czech Republic between 2016 and 2018. The ticks were pooled into 2591 groups of five and tested using duplex quantitative polymerase chain reaction (qPCR) for the presence of B. burgdorferi s.l. and B. miyamotoi. For each location, we estimated the overall prevalence of both agents using the EpiTools Epidemiological Calculator for pooled samples and calculated the minimum infection rate (MIR). To assess the potential risk of infection, we combined data on the abundance of nymphs and females with pathogen prevalence at each sampled site. Using a geographic information system (GIS), we mapped the MIR and infection risk of both Borrelia species across all 142 sampled locations and employed a geostatistical method (ordinary kriging) to predict MIR values and infection risk as continuous surfaces across the entire country.ResultsWe detected B. miyamotoi in 110 localities and B. burgdorferi s.l. in all 142 localities. The estimated prevalence of B. miyamotoi and B. burgdorferi s.l. in the collected ticks was 2.1% (95% confidence interval [CI] 1.8-2.3) and 27.1% (95% CI 26.0-28.3), respectively. For B. miyamotoi, we identified previously unknown, geographically distinct hotspots of MIR up to 8.3%, with MIR slightly higher in females (2.3%) than in males (1.9%) and nymphs (1.8%), though the difference was not statistically significant. In contrast, B. burgdorferi s.l. exhibited ubiquitous presence, with consistently high prevalence nationwide, showing similar MIRs in females (16.2%) and males (16.1%), and slightly lower in nymphs (15.6%). The highest infection risk for B. miyamotoi was 12.4 infected vectors per hour in southeastern Moravia, while the highest risk for B. burgdorferi s.l. reached 78.6 infected vectors per hour in the Bohemian-Moravian Highlands.ConclusionsBorrelia miyamotoi is widespread, forming distinct high-prevalence areas in certain regions. Borrelia burgdorferi s.l. demonstrates consistently high prevalence across most of the country, except for a few localized areas such as southwestern Czechia. Both pathogens exhibit natural nidality, forming regions with elevated prevalence and infection risk. Long-term time-series data are needed to confirm the spatio-temporal stability of these hotspots.

Project description:Borrelia burgdorferi and Borrelia miyamotoi are tick-vectored zoonotic pathogens maintained in wildlife species. Tick populations are establishing in new areas globally in response to climate change and other factors. New Brunswick is a Canadian maritime province at the advancing front of tick population establishment and has seen increasing numbers of ticks carrying B. burgdorferi, and more recently B. miyamotoi. Further, it is part of a region of Atlantic Canada with wildlife species composition differing from much of continental North America and little information exists as to the presence and frequency of infection of Borrelia spp. in wildlife in this region. We used a citizen science approach to collect a wide range of animals including migratory birds, medium-sized mammals, and small mammals. In total we tested 339 animals representing 20 species for the presence of B. burgdorferi and B. miyamotoi. We have developed new nested PCR primers and a protocol with excellent specificity for detecting both of these Borrelia species, both single and double infections, in tissues and organs of various wildlife species. The positive animals were primarily small non-migratory mammals, approximately twice as many were infected with B. burgdorferi than B. miyamotoi and one animal was found infected with both. In addition to established reservoir species, the jumping mouse (Napaeozapus insignis) was found frequently infected; this species had the highest infection prevalence for both B. burgdorferi and B. miyamotoi and has not previously been identified as an important carrier for either Borrelia species. Comprehensive testing of tissues found that all instances of B. burgdorferi infection were limited to one tissue within the host, whereas two of the five B. miyamotoi infections were diffuse and found in multiple systems. In the one coinfected specimen, two fetuses were also recovered and found infected with B. miyamotoi. This presumptive transplacental transmission suggests that vertical transmission in mammals is possible. This finding implies that B. miyamotoi could rapidly spread into wildlife populations, as well as having potential human health implications.

Project description:Borrelia burgdorferi sensu lato (s.l.) DNA was detected by PCR in Ixodes persulcatus Schulze, 1930, Haemaphysalis concinna Koch, 1844, Haemaphysalis japonica douglasi Nuttall et Warburton, 1915 and Dermacentor silvarum Olenev, 1932 ticks collected in the Amur region, the Jewish Autonomous region, the Sakhalin region and on the Khabarovsk territory. Infection rate of I. persulcatus with B. burgdorferi s.l. 10-69% exceeded the corresponding values of three other tick species in all examined regions during 1999-2014 despite different tick abundance and dominance structure. Bacterial loads estimated on the base of quantitative real time PCR varied from 102 to 109 genome-equivalents per a tick with maximal values for I. persulcatus and H. japonica. Phylogenetic analysis of 16S rRNA gene and 5S-23S rRNA intergenic spacer nucleotide sequences revealed two species: 1) Borrelia garinii of Asian type NT29 with several isolates of European type 20047; 2) Borrelia afzelii with identical sequences of the majority of studied isolates and VS461 reference strain in all regions except the Sakhalin Island where B. afzelii was not found. Borrelia miyamotoi of the relapsing fever group was detected as monoinfection or in combination with B. burgdorferi s.l. in 4.0 ± 0.9% and 4.8 ± 0.9% I. persulcatus ticks, respectively. Multiple locus sequence analysis of three fragments of 16S rRNA, glpQ and p66 genes proved that all the Far Eastern B. miyamotoi isolates belonged to the Asian type identical to FR64b strain (GenBank CP004217) from Japan. Wide distribution of Borrelia DNA in ticks, relative genetic homogeneity with similar sequences of the coding regions and the intergenic spacer of Borrelia wild isolates and temporal stability with high homology levels of the Far Eastern isolates of B. garinii, B. afzelii and B. miyamotoi with previously described spirochetes from the surrounding regions of Russia, China and Japan allowed us to suggest multiple ecological niches as the stability factor of the parasitic system.

Dataset Information

Hedgehogs, Squirrels, and Blackbirds as Sentinel Hosts for Active Surveillance of Borrelia miyamotoi and Borrelia burgdorferi Complex in Urban and Rural Environments.

Publications

Hedgehogs, Squirrels, and Blackbirds as Sentinel Hosts for Active Surveillance of <i>Borrelia miyamotoi</i> and <i>Borrelia burgdorferi</i> Complex in Urban and Rural Environments.

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