Abstract

Ticks carry numerous pathogens that, if transmitted, can cause disease in susceptible humans and animals. The present study describes our approach on how to investigate clinical presentations following tick bites in humans. To this aim, the occurrence of major tick-borne pathogens (TBPs) in human blood samples (n = 85) and the ticks collected (n = 93) from the same individuals were tested using an unbiased high-throughput pathogen detection microfluidic system. The clinical symptoms were characterized in enrolled patients. In patients with suspected TBP infection, serological assays were conducted to test for the presence of antibodies against specific TBPs. A field study based on One Health tenets was further designed to identify components of a potential chain of infection resulting in Rickettsia felis infection in one of the patients. Ticks species infesting humans were identified as Ixodes ricinus, Rhipicephalus sanguineus sensu lato (s.l.), Dermacentor reticulatus, and Haemaphysalis punctata. Five patients developed local skin lesions at the site of the tick bite including erythema migrans, local non-specific reactions, and cutaneous hypersensitivity reaction. Although Borrelia burgdorferi s.l., Babesia microti, Anaplasma phagocytophilum, and Candidatus Cryptoplasma sp. DNAs were detected in tick samples, different Rickettsia species were the most common TBPs identified in the ticks. The presence of TBPs such as Rickettsia helvetica, Rickettsia monacensis, Borrelia lusitaniae, Borrelia burgdorferi, Borrelia afzelii, A. phagocytophilum, and B. microti in ticks was further confirmed by DNA sequencing. Two of the patients with local skin lesions had IgG reactive against spotted fever group rickettsiae, while IgM specific to B. afzelii, Borrelia garinii, and Borrelia spielmanii were detected in the patient with erythema migrans. Although R. felis infection was detected in one human blood sample, none of the components of the potential chain of infection considered in this study tested positive to this pathogen either using direct pathogen detection in domestic dogs or xenodiagnosis in ticks collected from domestic cats. The combination of high-throughput screening of TBPs and One Health approaches might help characterize chains of infection leading to human infection by TBPs, as well as prevalence of emerging rickettsial pathogens in the Balkan region.

Highlights

  • Ticks (Ixodidae) are obligate blood-feeding ectoparasites of many animal hosts, including mammals, birds, and reptiles

  • The results based on molecular identification showed an overall infection prevalence of 68.82% with various tick-borne pathogens (TBPs) among the four ixodid tick species analyzed, including I. ricinus, R. sanguineus s.l., D. reticulatus, and H. punctata, which is in accordance with the average prevalence reported in a recent study from Serbia (Banovic et al, 2021b)

  • The frequency of detection of these microbes in ticks collected from the enrolled patients was unequal, Rickettsia spp. being the most common pathogen to which tick-infested humans could be exposed in Serbia

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Summary

Introduction

Ticks (Ixodidae) are obligate blood-feeding ectoparasites of many animal hosts, including mammals, birds, and reptiles. Western, and northern Europe, Ixodes ricinus, known as the castor bean tick, is the most widespread tick species (de la Fuente et al, 2017; Rosa et al, 2018). This species has been frequently reported to infest humans and is (Milutinovic et al, 2008b) the main vector for a large variety of TBPs transmitted to both humans and animals. Other tick species, such as the ornate cow tick Dermacentor reticulatus, the red sheep tick Haemaphysalis punctata, and the brown dog tick Rhipicephalus sanguineus s.l., are widely distributed across Europe where reports of tick bites by these species in human is increasing (Rubel et al, 2021)

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