Co-infection of Ticks: The Rule Rather Than the Exception
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Claire Valiente Moro ,Elise Vaumourin ,Lorraine Michelet ,Florence Hélène Tran ,Elodie Devillers ,
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Jean-François Cosson ,Patrick Gasqui ,Van Tran Van ,Patrick Mavingui ,Gwenaël Vourc’h ,Muriel Vayssier-Taussat
- Published: March 17, 2016
- DOI: 10.1371/journal.pntd.0004539
Abstract
Introduction
Ticks are the most common arthropod vectors of both human and animal diseases in Europe, and the
Ixodes ricinus
tick species is able to transmit a large number of bacteria, viruses
and parasites. Ticks may also be co-infected with several pathogens,
with a subsequent high likelihood of co-transmission to humans or
animals. However few data exist regarding co-infection prevalences, and
these studies only focus on certain well-known pathogens. In addition to
pathogens, ticks also carry symbionts that may play important roles in
tick biology, and could interfere with pathogen maintenance and
transmission. In this study we evaluated the prevalence of 38 pathogens
and four symbionts and their co-infection levels as well as possible
interactions between pathogens, or between pathogens and symbionts.
Methodology/principal findings
A total of 267
Ixodes ricinus
female specimens were collected in the French Ardennes and analyzed by
high-throughput real-time PCR for the presence of 37 pathogens (bacteria
and parasites), by rRT-PCR to detect the presence of Tick-Borne
encephalitis virus (TBEV) and by nested PCR to detect four symbionts.
Possible multipartite interactions between pathogens, or between
pathogens and symbionts were statistically evaluated. Among the infected
ticks, 45% were co-infected, and carried up to five different
pathogens. When adding symbiont prevalences, all ticks were infected by
at least one microorganism, and up to eight microorganisms were
identified in the same tick. When considering possible interactions
between pathogens, the results suggested a strong association between
Borrelia garinii and
B.
afzelii, whereas there were no significant interactions between symbionts and pathogens.
Conclusion/significance
Our
study reveals high pathogen co-infection rates in ticks, raising
questions about possible co-transmission of these agents to humans or
animals, and their consequences to human and animal health. We also
demonstrated high prevalence rates of symbionts co-existing with
pathogens, opening new avenues of enquiry regarding their effects on
pathogen transmission and vector competence.
Author Summary
Ticks
transmit more pathogens than any other arthropod, and one single
species can transmit a large variety of bacteria and parasites. Because
co-infection might be much more common than previously thought, we
evaluated the prevalence of 38 known or neglected tick-borne pathogens
in
Ixodes ricinus ticks. Our results demonstrated that
co-infection occurred in almost half of the infected ticks, and that
ticks could be infected with up to five pathogens. Moreover, as it is
well established that symbionts can affect pathogen transmission in
arthropods, we also evaluated the prevalence of four symbiont species
and demonstrated that all ticks were infected by at least one
microorganism. This work highlights the co-infection phenomenon in
ticks, which may have important implications for human and animal
health, emphasizing the need for new diagnostic tests better adapted to
tick-borne diseases. Finally, the high co-occurrence of symbionts and
pathogens in ticks, reveals the necessity to also account for these
interactions in the development of new alternative strategies to control
ticks and tick-borne disease.
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