An inverse association between West Nile virus serostatus and avian malaria infection status

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Abstract

Background

Various ecological and physiological mechanisms might influence the probability that two or more pathogens may simultaneously or sequentially infect a host individual. Concurrent infections can have important consequences for host condition and fitness, including elevated mortality risks. In addition, interactions between coinfecting pathogens may have important implications for transmission dynamics.

Methods

Here, we explore patterns of association between two common avian pathogens (West Nile virus and avian malaria parasites) among a suburban bird community in Chicago, IL, USA that share mosquito vectors. We surveyed 1714 individual birds across 13 species for both pathogens through established molecular protocols.

Results

Field investigations of haemosporidian and West Nile virus (WNV) infections among sampled birds yielded an inverse association between WNV serostatus and Plasmodium infection status. This relationship occurred in adult birds but not in juveniles. There was no evidence for a relationship between Haemoproteus infection and WNV serostatus. We detected similar prevalence of Plasmodium among birds captured with active WNV infections and spatiotemporally paired WNV-naïve individuals of the same species, demonstrating that the two pathogens can co-infect hosts.

Conclusions

Mechanisms explaining the negative association between WNV serostatus and Plasmodium infection status remain unclear and must be resolved through experimental infection procedures. However, our results highlight potential interactions between two common avian pathogens that may influence their transmission among hosts. This is especially relevant considering that West Nile virus is a common zoonotic pathogen with public health implications. Moreover, both pathogens are instructive models in infectious disease ecology, and infection with either has fitness consequences for their avian hosts.

Electronic supplementary material

The online version of this article (doi:10.1186/1756-3305-7-415) contains supplementary material, which is available to authorized users.

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Most cited references 49

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Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins.

T R Mosmann, H Cherwinski, M Bond … (1986)

A panel of antigen-specific mouse helper T cell clones was characterized according to patterns of lymphokine activity production, and two types of T cell were distinguished. Type 1 T helper cells (TH1) produced IL 2, interferon-gamma, GM-CSF, and IL 3 in response to antigen + presenting cells or to Con A, whereas type 2 helper T cells (TH2) produced IL 3, BSF1, and two other activities unique to the TH2 subset, a mast cell growth factor distinct from IL 3 and a T cell growth factor distinct from IL 2. Clones representing each type of T cell were characterized, and the pattern of lymphokine activities was consistent within each set. The secreted proteins induced by Con A were analyzed by biosynthetic labeling and SDS gel electrophoresis, and significant differences were seen between the two groups of T cell line. Both types of T cell grew in response to alternating cycles of antigen stimulation, followed by growth in IL 2-containing medium. Examples of both types of T cell were also specific for or restricted by the I region of the MHC, and the surface marker phenotype of the majority of both types was Ly-1+, Lyt-2-, L3T4+, Both types of helper T cell could provide help for B cells, but the nature of the help differed. TH1 cells were found among examples of T cell clones specific for chicken RBC and mouse alloantigens. TH2 cells were found among clones specific for mouse alloantigens, fowl gamma-globulin, and KLH. The relationship between these two types of T cells and previously described subsets of T helper cells is discussed.

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Experimental Infection of North American Birds with the New York 1999 Strain of West Nile Virus

Nicholas Komar, Stanley Langevin, Steven Hinten … (2003)

To evaluate transmission dynamics, we exposed 25 bird species to West Nile virus (WNV) by infectious mosquito bite. We monitored viremia titers, clinical outcome, WNV shedding (cloacal and oral), seroconversion, virus persistence in organs, and susceptibility to oral and contact transmission. Passeriform and charadriiform birds were more reservoir competent (a derivation of viremia data) than other species tested. The five most competent species were passerines: Blue Jay (Cyanocitta cristata), Common Grackle (Quiscalus quiscula), House Finch (Carpodacus mexicanus), American Crow (Corvus brachyrhynchos), and House Sparrow (Passer domesticus). Death occurred in eight species. Cloacal shedding of WNV was observed in 17 of 24 species, and oral shedding in 12 of 14 species. We observed contact transmission among four species and oral in five species. Persistent WNV infections were found in tissues of 16 surviving birds. Our observations shed light on transmission ecology of WNV and will benefit surveillance and control programs.

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Species interactions in a parasite community drive infection risk in a wildlife population.

Sandra Telfer, Xavier Lambin, Richard Birtles … (2010)

Most hosts, including humans, are simultaneously or sequentially infected with several parasites. A key question is whether patterns of coinfection arise because infection by one parasite species affects susceptibility to others or because of inherent differences between hosts. We used time-series data from individual hosts in natural populations to analyze patterns of infection risk for a microparasite community, detecting large positive and negative effects of other infections. Patterns remain once variations in host susceptibility and exposure are accounted for. Indeed, effects are typically of greater magnitude, and explain more variation in infection risk, than the effects associated with host and environmental factors more commonly considered in disease studies. We highlight the danger of mistaken inference when considering parasite species in isolation rather than parasite communities.

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Author and article information

Contributors

Matthew CI Medeiros: mcmn92@umsl.edu

Tavis K Anderson: tkanderson@georgiasouthern.edu

Uriel D Kitron: ukitron@emory.edu

Edward D Walker: walker@msu.edu

Jeffrey D Brawn: jbrawn@illinois.edu

Bethany L Krebs: krebs2@illinois.edu

Marilyn O Ruiz: moruiz@illinois.edu

Tony L Goldberg: tgoldberg@vetmed.wisc.edu

Robert E Ricklefs: ricklefs@umsl.edu

Gabriel L Hamer: ghamer@tamu.edu

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 1 September 2014

Publication date PMC-release: 1 September 2014

Publication date Collection: 2014

Volume: 7

Issue: 1

Electronic Location Identifier: 415

Affiliations

[ ]Department of Biology, University of Missouri-St. Louis, One University Boulevard, St. Louis, MO 63121 USA

[ ]Department of Biology, Georgia Southern University, P.O. Box 8042–1, Statesboro, 30460 Georgia

[ ]Department of Environmental Studies, Emory University, 400 Dowman Drive, Atlanta, GA 30322 USA

[ ]Department of Microbiology and Molecular Genetics, 2215 Biomedical Physical Sciences East, Lansing, MI 48824-4320 USA

[ ]Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 South Goodwin Ave., Urbana, IL 61801 USA

[ ]Department of Pathobiology, University of Illinois, 2001 S. Lincoln, Urbana, IL 61801 USA

[ ]Department of Pathobiological Sciences, University of Wisconsin, 2015 Linden Dr., Madison, WI 53706 USA

[ ]Department of Entomology, Texas A&M University, 2475 TAMU, College Station, TX 77843-2475 USA

Article

Publisher ID: 1597

DOI: 10.1186/1756-3305-7-415

PMC ID: 4262112

PubMed ID: 25178911

SO-VID: 2e7bdf92-4669-4f90-881b-ac4676b2fd6c

License:

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 24 June 2014

Date accepted : 20 August 2014

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: parasite-parasite interactions,coinfection,concurrent infection,concomitant infection,west nile virus,haemosporida,avian malaria

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: parasite-parasite interactions, coinfection, concurrent infection, concomitant infection, west nile virus, haemosporida, avian malaria

An inverse association between West Nile virus serostatus and avian malaria infection status

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Abstract

Background

Methods

Results

Conclusions

Electronic supplementary material

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Decoding Infection and Transmission

Most cited references 49

Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins.

Experimental Infection of North American Birds with the New York 1999 Strain of West Nile Virus

Species interactions in a parasite community drive infection risk in a wildlife population.

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