Cargando…

Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome

The apicomplexan parasite Toxoplasma gondii, the causative agent of toxoplasmosis, can infect all warm-blooded animals. T. gondii can subtly alter host behaviors—either through manipulation to enhance transmission to the feline definitive host or as a side-effect, or “constraint,” of infection. In h...

Descripción completa

Detalles Bibliográficos
Autores principales: Milne, Gregory, Fujimoto, Chelsea, Bean, Theodor, Peters, Harry J., Hemmington, Martin, Taylor, Charly, Fowkes, Robert C., Martineau, Henny M., Hamilton, Clare M., Walker, Martin, Mitchell, Judy A., Léger, Elsa, Priestnall, Simon L., Webster, Joanne P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7525129/
https://www.ncbi.nlm.nih.gov/pubmed/33192643
http://dx.doi.org/10.3389/fpsyt.2020.513536
_version_ 1783588678862372864
author Milne, Gregory
Fujimoto, Chelsea
Bean, Theodor
Peters, Harry J.
Hemmington, Martin
Taylor, Charly
Fowkes, Robert C.
Martineau, Henny M.
Hamilton, Clare M.
Walker, Martin
Mitchell, Judy A.
Léger, Elsa
Priestnall, Simon L.
Webster, Joanne P.
author_facet Milne, Gregory
Fujimoto, Chelsea
Bean, Theodor
Peters, Harry J.
Hemmington, Martin
Taylor, Charly
Fowkes, Robert C.
Martineau, Henny M.
Hamilton, Clare M.
Walker, Martin
Mitchell, Judy A.
Léger, Elsa
Priestnall, Simon L.
Webster, Joanne P.
author_sort Milne, Gregory
collection PubMed
description The apicomplexan parasite Toxoplasma gondii, the causative agent of toxoplasmosis, can infect all warm-blooded animals. T. gondii can subtly alter host behaviors—either through manipulation to enhance transmission to the feline definitive host or as a side-effect, or “constraint,” of infection. In humans, T. gondii infection, either alone or in association with other co-infecting neurotropic agents, has been reliably associated with both subtle behavioral changes and, in some cases, severe neuropsychiatric disorders, including schizophrenia. Research on the potential impact of T. gondii on the behavior of other long-lived naturally infected hosts is lacking. Recent studies reported a large number of wild red foxes exhibiting a range of aberrant behavioral traits, subsequently classified as Dopey Fox Syndrome (DFS). Here we assessed the potential association between T. gondii and/or other neurotropic agents with DFS. Live, captive foxes within welfare centers were serologically tested for T. gondii and, if they died naturally, PCR-tested for vulpine circovirus (FoxCV). Post-mortem pseudo-control wild foxes, obtained from pest management companies, were PCR-tested for T. gondii, FoxCV, canine distemper virus (CDV), canine adenovirus type (CAV)-1 and CAV-2. We also assessed, using non-invasive assays, whether T. gondii–infected foxes showed subtle behavioral alterations as observed among infected rodent (and other) hosts, including altered activity, risk, and stress levels. All foxes tested negative for CAV, CDV, CHV, and DogCV. DFS was found to be associated with singular T. gondii infection (captives vs. pseudo-controls, 33.3% (3/9) vs. 6.8% (5/74)) and singular FoxCV infection (66.7% (6/9) vs. 11.1% (1/9)) and with T. gondii/FoxCV co-infection (33.3% (3/9) vs. 11.1% (1/9)). Overall, a higher proportion of captive foxes had signs of neuroinflammation compared to pseudo-controls (66.7% (4/6) vs. 11.1% (1/9)). Consistent with behavioral changes seen in infected rodents, T. gondii–infected foxes displayed increased attraction toward feline odor (n=6 foxes). These preliminary results suggest that wild foxes with DFS are infected with T. gondii and likely co-infected with FoxCV and/or another co-infecting neurotropic agent. Our findings using this novel system have important implications for our understanding of both the impact of parasites on mammalian host behavior in general and, potentially, of the infectious causation of certain neuropsychiatric disorders.
format Online
Article
Text
id pubmed-7525129
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-75251292020-11-13 Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome Milne, Gregory Fujimoto, Chelsea Bean, Theodor Peters, Harry J. Hemmington, Martin Taylor, Charly Fowkes, Robert C. Martineau, Henny M. Hamilton, Clare M. Walker, Martin Mitchell, Judy A. Léger, Elsa Priestnall, Simon L. Webster, Joanne P. Front Psychiatry Psychiatry The apicomplexan parasite Toxoplasma gondii, the causative agent of toxoplasmosis, can infect all warm-blooded animals. T. gondii can subtly alter host behaviors—either through manipulation to enhance transmission to the feline definitive host or as a side-effect, or “constraint,” of infection. In humans, T. gondii infection, either alone or in association with other co-infecting neurotropic agents, has been reliably associated with both subtle behavioral changes and, in some cases, severe neuropsychiatric disorders, including schizophrenia. Research on the potential impact of T. gondii on the behavior of other long-lived naturally infected hosts is lacking. Recent studies reported a large number of wild red foxes exhibiting a range of aberrant behavioral traits, subsequently classified as Dopey Fox Syndrome (DFS). Here we assessed the potential association between T. gondii and/or other neurotropic agents with DFS. Live, captive foxes within welfare centers were serologically tested for T. gondii and, if they died naturally, PCR-tested for vulpine circovirus (FoxCV). Post-mortem pseudo-control wild foxes, obtained from pest management companies, were PCR-tested for T. gondii, FoxCV, canine distemper virus (CDV), canine adenovirus type (CAV)-1 and CAV-2. We also assessed, using non-invasive assays, whether T. gondii–infected foxes showed subtle behavioral alterations as observed among infected rodent (and other) hosts, including altered activity, risk, and stress levels. All foxes tested negative for CAV, CDV, CHV, and DogCV. DFS was found to be associated with singular T. gondii infection (captives vs. pseudo-controls, 33.3% (3/9) vs. 6.8% (5/74)) and singular FoxCV infection (66.7% (6/9) vs. 11.1% (1/9)) and with T. gondii/FoxCV co-infection (33.3% (3/9) vs. 11.1% (1/9)). Overall, a higher proportion of captive foxes had signs of neuroinflammation compared to pseudo-controls (66.7% (4/6) vs. 11.1% (1/9)). Consistent with behavioral changes seen in infected rodents, T. gondii–infected foxes displayed increased attraction toward feline odor (n=6 foxes). These preliminary results suggest that wild foxes with DFS are infected with T. gondii and likely co-infected with FoxCV and/or another co-infecting neurotropic agent. Our findings using this novel system have important implications for our understanding of both the impact of parasites on mammalian host behavior in general and, potentially, of the infectious causation of certain neuropsychiatric disorders. Frontiers Media S.A. 2020-09-16 /pmc/articles/PMC7525129/ /pubmed/33192643 http://dx.doi.org/10.3389/fpsyt.2020.513536 Text en Copyright © 2020 Milne, Fujimoto, Bean, Peters, Hemmington, Taylor, Fowkes, Martineau, Hamilton, Walker, Mitchell, Léger, Priestnall and Webster http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychiatry
Milne, Gregory
Fujimoto, Chelsea
Bean, Theodor
Peters, Harry J.
Hemmington, Martin
Taylor, Charly
Fowkes, Robert C.
Martineau, Henny M.
Hamilton, Clare M.
Walker, Martin
Mitchell, Judy A.
Léger, Elsa
Priestnall, Simon L.
Webster, Joanne P.
Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title_full Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title_fullStr Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title_full_unstemmed Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title_short Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome
title_sort infectious causation of abnormal host behavior: toxoplasma gondii and its potential association with dopey fox syndrome
topic Psychiatry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7525129/
https://www.ncbi.nlm.nih.gov/pubmed/33192643
http://dx.doi.org/10.3389/fpsyt.2020.513536
work_keys_str_mv AT milnegregory infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT fujimotochelsea infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT beantheodor infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT petersharryj infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT hemmingtonmartin infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT taylorcharly infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT fowkesrobertc infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT martineauhennym infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT hamiltonclarem infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT walkermartin infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT mitchelljudya infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT legerelsa infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT priestnallsimonl infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome
AT websterjoannep infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome