Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus

Abstract Background Reliable information on host use by arthropod vectors is required to study pathogen transmission ecology and to predict disease risk. Direct observation of host use is often difficult or impossible and indirect methods are therefore necessary. However, the reliability of currentl...

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Main Authors: Elsa Léger, Xiangye Liu, Sébastien Masseglia, Valérie Noël, Gwenaël Vourc’h, Sarah Bonnet, Karen D. McCoy
Format: Article
Language:English
Published: BMC 2015-08-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-015-1043-7
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author Elsa Léger
Xiangye Liu
Sébastien Masseglia
Valérie Noël
Gwenaël Vourc’h
Sarah Bonnet
Karen D. McCoy
author_facet Elsa Léger
Xiangye Liu
Sébastien Masseglia
Valérie Noël
Gwenaël Vourc’h
Sarah Bonnet
Karen D. McCoy
author_sort Elsa Léger
collection DOAJ
description Abstract Background Reliable information on host use by arthropod vectors is required to study pathogen transmission ecology and to predict disease risk. Direct observation of host use is often difficult or impossible and indirect methods are therefore necessary. However, the reliability of currently available methods to identify the last host of blood-feeding arthropods has not been evaluated, and may be particularly problematic for ticks because host blood has been digested at capture. Biases in host detection may lead to erroneous conclusions on both vector ecology and pathogen circulation. Methods Here, we experimentally tested for biases in host detection using the generalist three-host tick Ixodes ricinus as a model system. We fed ticks using an artificial feeding system and amplified blood meal traces post-moult (i.e., in the succeeding unfed life stage) via both a quantitative real-time polymerase chain reaction assay and a reverse line blotting method. We then experimentally tested for three types of biases in host detection: 1) time post-moult, 2) tick life stage and 3) host type (non-nucleated mammal blood versus nucleated avian blood), and compared these biases between the two molecular methods. Results Our results show that all three factors can influence host detection in ticks but not necessarily in the expected way. Although host detection rates decreased with time post-moult, mammal blood tended to be more readily detected than bird blood. Tick life stage was also an important factor; detection was higher in nymphs than in adults and, in some cases, remnants from both larval and nymphal blood meals could be detected in the adult stage. These biases were similar for the two detection techniques. Conclusions We show that different factors associated with questing ticks may influence our ability to correctly infer previous host use and that these factors may bias inferences from field-based studies. As these biases may be common to other vector-borne disease systems, their implications for our understanding of vector ecology and disease transmission require more explicit consideration.
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spelling doaj.art-2a105e9489cd4297884e7339e7b955572023-06-04T11:12:43ZengBMCParasites & Vectors1756-33052015-08-018111010.1186/s13071-015-1043-7Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinusElsa Léger0Xiangye Liu1Sébastien Masseglia2Valérie Noël3Gwenaël Vourc’h4Sarah Bonnet5Karen D. McCoy6MIVEGEC (UMR UM2-UM1-CNRS 5290, UR IRD 224), Centre IRDUSC INRA Bartonella-tiques, UMR BIPAR ENVA-ANSESUnité Epidémiologie Animale (UR INRA 346), Centre de recherche INRA de Clermont-Ferrand / TheixMIVEGEC (UMR UM2-UM1-CNRS 5290, UR IRD 224), Centre IRDUnité Epidémiologie Animale (UR INRA 346), Centre de recherche INRA de Clermont-Ferrand / TheixUSC INRA Bartonella-tiques, UMR BIPAR ENVA-ANSESMIVEGEC (UMR UM2-UM1-CNRS 5290, UR IRD 224), Centre IRDAbstract Background Reliable information on host use by arthropod vectors is required to study pathogen transmission ecology and to predict disease risk. Direct observation of host use is often difficult or impossible and indirect methods are therefore necessary. However, the reliability of currently available methods to identify the last host of blood-feeding arthropods has not been evaluated, and may be particularly problematic for ticks because host blood has been digested at capture. Biases in host detection may lead to erroneous conclusions on both vector ecology and pathogen circulation. Methods Here, we experimentally tested for biases in host detection using the generalist three-host tick Ixodes ricinus as a model system. We fed ticks using an artificial feeding system and amplified blood meal traces post-moult (i.e., in the succeeding unfed life stage) via both a quantitative real-time polymerase chain reaction assay and a reverse line blotting method. We then experimentally tested for three types of biases in host detection: 1) time post-moult, 2) tick life stage and 3) host type (non-nucleated mammal blood versus nucleated avian blood), and compared these biases between the two molecular methods. Results Our results show that all three factors can influence host detection in ticks but not necessarily in the expected way. Although host detection rates decreased with time post-moult, mammal blood tended to be more readily detected than bird blood. Tick life stage was also an important factor; detection was higher in nymphs than in adults and, in some cases, remnants from both larval and nymphal blood meals could be detected in the adult stage. These biases were similar for the two detection techniques. Conclusions We show that different factors associated with questing ticks may influence our ability to correctly infer previous host use and that these factors may bias inferences from field-based studies. As these biases may be common to other vector-borne disease systems, their implications for our understanding of vector ecology and disease transmission require more explicit consideration.https://doi.org/10.1186/s13071-015-1043-7Host identificationHematophagous arthropodsIxodidaeMolecular methodsDetection biasesVector-borne diseases
spellingShingle Elsa Léger
Xiangye Liu
Sébastien Masseglia
Valérie Noël
Gwenaël Vourc’h
Sarah Bonnet
Karen D. McCoy
Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
Parasites & Vectors
Host identification
Hematophagous arthropods
Ixodidae
Molecular methods
Detection biases
Vector-borne diseases
title Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
title_full Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
title_fullStr Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
title_full_unstemmed Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
title_short Reliability of molecular host-identification methods for ticks: an experimental in vitro study with Ixodes ricinus
title_sort reliability of molecular host identification methods for ticks an experimental in vitro study with ixodes ricinus
topic Host identification
Hematophagous arthropods
Ixodidae
Molecular methods
Detection biases
Vector-borne diseases
url https://doi.org/10.1186/s13071-015-1043-7
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