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...
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-09-01
|
| Series: | Frontiers in Psychiatry |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpsyt.2020.513536/full |
| _version_ | 1819227419380285440 |
|---|---|
| author | Gregory Milne Gregory Milne Chelsea Fujimoto Theodor Bean Harry J. Peters Martin Hemmington Charly Taylor Robert C. Fowkes Henny M. Martineau Clare M. Hamilton Martin Walker Martin Walker Judy A. Mitchell Elsa Léger Elsa Léger Simon L. Priestnall Joanne P. Webster Joanne P. Webster |
| author_facet | Gregory Milne Gregory Milne Chelsea Fujimoto Theodor Bean Harry J. Peters Martin Hemmington Charly Taylor Robert C. Fowkes Henny M. Martineau Clare M. Hamilton Martin Walker Martin Walker Judy A. Mitchell Elsa Léger Elsa Léger Simon L. Priestnall Joanne P. Webster Joanne P. Webster |
| author_sort | Gregory Milne |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-23T10:41:05Z |
| format | Article |
| id | doaj.art-54f32a865c4849ed88f0f9c960aa5375 |
| institution | Directory Open Access Journal |
| issn | 1664-0640 |
| language | English |
| last_indexed | 2024-12-23T10:41:05Z |
| publishDate | 2020-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Psychiatry |
| spelling | doaj.art-54f32a865c4849ed88f0f9c960aa53752022-12-21T17:50:10ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402020-09-011110.3389/fpsyt.2020.513536513536Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox SyndromeGregory Milne0Gregory Milne1Chelsea Fujimoto2Theodor Bean3Harry J. Peters4Martin Hemmington5Charly Taylor6Robert C. Fowkes7Henny M. Martineau8Clare M. Hamilton9Martin Walker10Martin Walker11Judy A. Mitchell12Elsa Léger13Elsa Léger14Simon L. Priestnall15Joanne P. Webster16Joanne P. Webster17Department of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomLondon Centre for Neglected Tropical Disease Research, Imperial College London Faculty of Medicine, London, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomNational Fox Welfare Society, Rushden, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomParasitology Division, Moredun Research Institute, Edinburgh, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomLondon Centre for Neglected Tropical Disease Research, Imperial College London Faculty of Medicine, London, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomLondon Centre for Neglected Tropical Disease Research, Imperial College London Faculty of Medicine, London, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomDepartment of Pathobiology and Population Sciences, Royal Veterinary College, University of London, Hatfield, United KingdomLondon Centre for Neglected Tropical Disease Research, Imperial College London Faculty of Medicine, London, United KingdomThe 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.https://www.frontiersin.org/article/10.3389/fpsyt.2020.513536/fullneurotropicinflammationfoxhostschizophreniaToxoplasma gondii |
| spellingShingle | Gregory Milne Gregory Milne Chelsea Fujimoto Theodor Bean Harry J. Peters Martin Hemmington Charly Taylor Robert C. Fowkes Henny M. Martineau Clare M. Hamilton Martin Walker Martin Walker Judy A. Mitchell Elsa Léger Elsa Léger Simon L. Priestnall Joanne P. Webster Joanne P. Webster Infectious Causation of Abnormal Host Behavior: Toxoplasma gondii and Its Potential Association With Dopey Fox Syndrome Frontiers in Psychiatry neurotropic inflammation fox host schizophrenia Toxoplasma gondii |
| 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 | neurotropic inflammation fox host schizophrenia Toxoplasma gondii |
| url | https://www.frontiersin.org/article/10.3389/fpsyt.2020.513536/full |
| work_keys_str_mv | AT gregorymilne infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT gregorymilne infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT chelseafujimoto infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT theodorbean infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT harryjpeters infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT martinhemmington infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT charlytaylor infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT robertcfowkes infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT hennymmartineau infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT claremhamilton infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT martinwalker infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT martinwalker infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT judyamitchell infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT elsaleger infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT elsaleger infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT simonlpriestnall infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT joannepwebster infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome AT joannepwebster infectiouscausationofabnormalhostbehaviortoxoplasmagondiianditspotentialassociationwithdopeyfoxsyndrome |