Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks

Abstract Background The bacterium Coxiella burnetii is the etiological agent of Q fever and is mainly transmitted via inhalation of infectious aerosols. DNA of C. burnetii is frequently detected in ticks, but the role of ticks as vectors in the epidemiology of this agent is still controversial. In t...

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Main Authors: Sophia Körner, Gustavo R. Makert, Katja Mertens-Scholz, Klaus Henning, Martin Pfeffer, Alexander Starke, Ard M. Nijhof, Sebastian Ulbert
Format: Article
Language:English
Published: BMC 2020-02-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-020-3956-z
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spelling doaj-3d682854019646439edd926b78b203d82021-02-14T12:10:51ZengBMCParasites & Vectors1756-33052020-02-0113111110.1186/s13071-020-3956-zUptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticksSophia Körner0Gustavo R. Makert1Katja Mertens-Scholz2Klaus Henning3Martin Pfeffer4Alexander Starke5Ard M. Nijhof6Sebastian Ulbert7Department of Immunology, Fraunhofer Institute for Cell Therapy and ImmunologyDepartment of Immunology, Fraunhofer Institute for Cell Therapy and ImmunologyInstitute of Bacterial Infections and Zoonoses (IBIZ), Friedrich-Loeffler-Institut, Federal Research Institute for Animal HealthInstitute of Bacterial Infections and Zoonoses (IBIZ), Friedrich-Loeffler-Institut, Federal Research Institute for Animal HealthInstitute of Animal Hygiene and Veterinary Public Health, University of LeipzigClinic for Ruminants and Swine, Faculty of Veterinary Medicine, University of LeipzigInstitute for Parasitology and Tropical Veterinary Medicine, Freie Universität BerlinDepartment of Immunology, Fraunhofer Institute for Cell Therapy and ImmunologyAbstract Background The bacterium Coxiella burnetii is the etiological agent of Q fever and is mainly transmitted via inhalation of infectious aerosols. DNA of C. burnetii is frequently detected in ticks, but the role of ticks as vectors in the epidemiology of this agent is still controversial. In this study, Ixodes ricinus and Dermacentor marginatus adults as well as I. ricinus nymphs were fed on blood spiked with C. burnetii in order to study the fate of the bacterium within putative tick vectors. Methods Blood-feeding experiments were performed in vitro in silicone-membrane based feeding units. The uptake, fecal excretion and transstadial transmission of C. burnetii was examined by quantitative real-time PCR as well as cultivation of feces and crushed tick filtrates in L-929 mouse fibroblast cells and cell-free culture medium. Results Ticks successfully fed in the feeding system with engorgement rates ranging from 29% (D. marginatus) to 64% (I. ricinus adults). Coxiella burnetii DNA was detected in the feces of both tick species during and after feeding on blood containing 105 or 106 genomic equivalents per ml blood (GE/ml), but not when fed on blood containing only 104 GE/ml. Isolation and cultivation demonstrated the infectivity of C. burnetii in shed feces. In 25% of the I. ricinus nymphs feeding on inoculated blood, a transstadial transmission to the adult stage was detected. Females that molted from nymphs fed on inoculated blood excreted C. burnetii of up to 106 genomic equivalents per mg of feces. Conclusions These findings show that transstadial transmission of C. burnetii occurs in I. ricinus and confirm that I. ricinus is a potential vector for Q fever. Transmission from both tick species might occur by inhalation of feces containing high amounts of viable C. burnetii rather than via tick bites.https://doi.org/10.1186/s13071-020-3956-zCoxiella burnetiiTicksTransmission
collection DOAJ
language English
format Article
sources DOAJ
author Sophia Körner
Gustavo R. Makert
Katja Mertens-Scholz
Klaus Henning
Martin Pfeffer
Alexander Starke
Ard M. Nijhof
Sebastian Ulbert
spellingShingle Sophia Körner
Gustavo R. Makert
Katja Mertens-Scholz
Klaus Henning
Martin Pfeffer
Alexander Starke
Ard M. Nijhof
Sebastian Ulbert
Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
Parasites & Vectors
Coxiella burnetii
Ticks
Transmission
author_facet Sophia Körner
Gustavo R. Makert
Katja Mertens-Scholz
Klaus Henning
Martin Pfeffer
Alexander Starke
Ard M. Nijhof
Sebastian Ulbert
author_sort Sophia Körner
title Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
title_short Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
title_full Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
title_fullStr Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
title_full_unstemmed Uptake and fecal excretion of Coxiella burnetii by Ixodes ricinus and Dermacentor marginatus ticks
title_sort uptake and fecal excretion of coxiella burnetii by ixodes ricinus and dermacentor marginatus ticks
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2020-02-01
description Abstract Background The bacterium Coxiella burnetii is the etiological agent of Q fever and is mainly transmitted via inhalation of infectious aerosols. DNA of C. burnetii is frequently detected in ticks, but the role of ticks as vectors in the epidemiology of this agent is still controversial. In this study, Ixodes ricinus and Dermacentor marginatus adults as well as I. ricinus nymphs were fed on blood spiked with C. burnetii in order to study the fate of the bacterium within putative tick vectors. Methods Blood-feeding experiments were performed in vitro in silicone-membrane based feeding units. The uptake, fecal excretion and transstadial transmission of C. burnetii was examined by quantitative real-time PCR as well as cultivation of feces and crushed tick filtrates in L-929 mouse fibroblast cells and cell-free culture medium. Results Ticks successfully fed in the feeding system with engorgement rates ranging from 29% (D. marginatus) to 64% (I. ricinus adults). Coxiella burnetii DNA was detected in the feces of both tick species during and after feeding on blood containing 105 or 106 genomic equivalents per ml blood (GE/ml), but not when fed on blood containing only 104 GE/ml. Isolation and cultivation demonstrated the infectivity of C. burnetii in shed feces. In 25% of the I. ricinus nymphs feeding on inoculated blood, a transstadial transmission to the adult stage was detected. Females that molted from nymphs fed on inoculated blood excreted C. burnetii of up to 106 genomic equivalents per mg of feces. Conclusions These findings show that transstadial transmission of C. burnetii occurs in I. ricinus and confirm that I. ricinus is a potential vector for Q fever. Transmission from both tick species might occur by inhalation of feces containing high amounts of viable C. burnetii rather than via tick bites.
topic Coxiella burnetii
Ticks
Transmission
url https://doi.org/10.1186/s13071-020-3956-z
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