Borrelia Diversity and Co-infection with Other Tick Borne Pathogens in Ticks.

Gheorghe Savuta,Sara Moutailler,Andrei D. Mihalca,Muriel Vayssier-Taussat,Daniela Porea,Ionuţ Pavel,Cristian Raileanu

doi:10.3389/fcimb.2017.00036

Abstract

Identifying Borrelia burgdorferi as the causative agent of Lyme disease in 1981 was a watershed moment in understanding the major impact that tick-borne zoonoses can have on public health worldwide, particularly in Europe and the USA. The medical importance of tick-borne diseases has long since been acknowledged, yet little is known regarding the occurrence of emerging tick-borne pathogens such as Borrelia spp., Anaplasma phagocytophilum, Rickettsia spp., Bartonella spp., “Candidatus Neoehrlichia mikurensis”, and tick-borne encephalitis virus in questing ticks in Romania, a gateway into Europe. The objective of our study was to identify the infection and co-infection rates of different Borrelia genospecies along with other tick-borne pathogens in questing ticks collected from three geographically distinct areas in eastern Romania. We collected 557 questing adult and nymph ticks of three different species (534 Ixodes ricinus, 19 Haemaphysalis punctata, and 4 Dermacentor reticulatus) from three areas in Romania. We analyzed ticks individually for the presence of eight different Borrelia genospecies with high-throughput real-time PCR. Ticks with Borrelia were then tested for possible co-infections with A. phagocytophilum, Rickettsia spp., Bartonella spp., “Candidatus Neoehrlichia mikurensis”, and tick-borne encephalitis virus. Borrelia spp. was detected in I. ricinus ticks from all sampling areas, with global prevalence rates of 25.8%. All eight Borrelia genospecies were detected in I. ricinus ticks: Borrelia garinii (14.8%), B. afzelii (8.8%), B. valaisiana (5.1%), B. lusitaniae (4.9%), B. miyamotoi (0.9%), B. burgdorferi s.s (0.4%), and B. bissettii (0.2%). Regarding pathogen co-infection 64.5% of infected I. ricinus were positive for more than one pathogen. Associations between different Borrelia genospecies were detected in 9.7% of ticks, and 6.9% of I. ricinus ticks tested positive for co-infection of Borrelia spp. with other tick-borne pathogens. The most common association was between B. garinii and B. afzelii (4.3%), followed by B. garinii and B. lusitaniae (3.0%). The most frequent dual co-infections were between Borrelia spp. and Rickettsia spp., (1.3%), and between Borrelia spp. and “Candidatus Neoehrlichia mikurensis” (1.3%). The diversity of tick-borne pathogens detected in this study and the frequency of co-infections should influence all infection risk evaluations following a tick bite.

Highlights

In Europe, ticks are the most ecologically important vectors of pathogens that cause both human and animal diseases (de la Fuente et al, 2008)
Our objective was to identify infection rates for different Borrelia genospecies along with other tick-borne pathogens in questing ticks collected from three sites in eastern Romania: One urban region dedicated to recreational activities and two forested areas
Using a powerful high-throughput tool we performed a comprehensive overview of the epidemiological status of Lyme spirochetes circulating and co-circulating with other important tick-borne pathogens in eastern Romanian ticks

Summary

Introduction

In Europe, ticks are the most ecologically important vectors of pathogens that cause both human and animal diseases (de la Fuente et al, 2008). Ixodes ricinus ticks are the most common ticks in Europe, and are broadly distributed across the entire continent They are capable of transmitting a wide variety of zoonotic pathogens, such as viruses, bacteria, protozoa, and even helminths (Egyed et al, 2012). Five genospecies are human pathogens: B. afzelii, B. garinii, B. burgdorferi sensu stricto (s.s.), B. bavariensis, and B. spielmanii; three are suspected human pathogens: B. lusitaniae, B. valaisiana, and B. finlandensis; and one genospecies, B. bissettii, has no clinical relevance to humans Another Borrelia genospecies, Borrelia miyamotoi, belongs to the relapsing fever group and is transmitted by the same Ixodes species that transmits B. burgdorferi s.l. In 2013 B. miyamotoi was identified as a human pathogen in Europe (Hovius et al, 2013). This bacterium has been recently identified in Romania (Kalmár et al, 2016)

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