Parasitic manipulation or side effects? The effects of past Toxoplasma gondii and Borrelia spp. infections on human personality and cognitive performance are not mediated by impaired health.

behaviour borreliosis manipulation hypothesis personality side effects hypothesis toxoplasmosis

Journal

Folia parasitologica
ISSN: 1803-6465
Titre abrégé: Folia Parasitol (Praha)
Pays: Czech Republic
ID NLM: 0065750

Informations de publication

Date de publication:
28 Nov 2023
Historique:
received: 13 06 2023
accepted: 31 10 2023
medline: 12 12 2023
pubmed: 12 12 2023
entrez: 12 12 2023
Statut: epublish

Résumé

Bacteria Borrelia burgdorferi s. l. and even more the protist Toxoplasma gondii Nicolle et Manceaux, 1908, are known to affect the behaviour and mental health of their animal and human hosts. Both pathogens infect a significant fraction of human population, both are neurotropic and survive in the host's body for a long time. While latent infections were thought to be clinically asymptomatic, recent studies suggest otherwise, revealing adverse effects on human health. It was hypothesised that the specific behavioural effects of these pathogens may be side effects of general health impairments in infected individuals. This hypothesis was tested using about one hour-long survey consisting of questionnaires and performance tests on a cohort of 7,762 members of the internet population. Results showed that individuals infected with T. gondii reported worse physical and mental health, and those infected with Borrelia spp. reported worse physical health than uninfected controls. Furthermore, infected and noninfected individuals differed in several personality traits, including conscientiousness, pathogen disgust, injury disgust, Machiavellianism, narcissism, tribalism, anti-authoritarianism, intelligence, reaction time, and precision. While the majority of behavioural effects associated with Borrelia infection were similar to those associated with Toxoplasma infection, some differences were observed, such as performance in the Stroop test. Path analyses and nonparametric partial Kendall correlation tests showed that these effects were not mediated by impaired health in infected individuals, contradicting the side effects hypothesis.

Identifiants

pubmed: 38084079
doi: 10.14411/fp.2023.020
doi:
pii:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Références

Angyal A. 1941: Disgust and related aversions. J. Abnorm. Soc. Psychol. 36: 393-412.
doi: 10.1037/h0058254
Aruguete M.S., Huynh H., Browne B.L., Jurs B., Flint E., McCutcheon L.E. 2019: How serious is the 'carelessness' problem on Mechanical Turk? Int. J. Soc. Res. Methodol. 22: 441-449.
doi: 10.1080/13645579.2018.1563966
Berdoy M., Webster J.P., Macdonald D.W. 1995: The manipulation of rat behaviour by Toxoplasma gondii. Mammalia 59: 605-613.
doi: 10.1515/mamm.1995.59.4.605
Bransfield R.C. 2018a: Neuropsychiatric Lyme borreliosis: an overview with a focus on a specialty psychiatrist's clinical practice. Healthcare 6: 23.
doi: 10.3390/healthcare6030104
Bransfield R.C. 2018b: Aggressiveness, violence, homicidality, homicide, and Lyme disease. Neuropsychiatr. Dis. Treat. 14: 693-713.
doi: 10.2147/NDT.S155143
Carney W.P. 1969: Behavioral and morphological changes in carpenter ants harboring dicrocoeliid metacercariae. Am. Midl. Nat. 82: 605-611.
doi: 10.2307/2423801
Cattell H.E.P., Mead A.D. 2008: The Sixteen Personality Factor Questionnaire (16PF). In: G.J. Boyle, G.M.D. Saklofske (Eds.), The Sage Handbook of Personality Theory and Assessment. Sage Publications, Los Angeles, pp. 295-312.
doi: 10.4135/9781849200479.n7
Cezilly F., Thomas F., Medoc V., Perrot-Minnot M.J. 2010: Host-manipulation by parasites with complex life cycles: adaptive or not? Trends Parasitol. 26: 311-317.
doi: 10.1016/j.pt.2010.03.009
Coccaro E.F., Lee R., Groer M.W., Can A., Coussons-Read M., Postolache, T.T. 2016: Toxoplasma gondii infection: relationship with aggression in psychiatric subjects. J. Clin. Psychiatry 77: 334-341.
doi: 10.4088/JCP.14m09621
Fallon B.A., Nields J.A., Burrascano J.J., Liegner K., DelBene D., Liebowitz M.R. 1992. The neuropsychiatric manifestations of Lyme borreliosis. Psychiatric Q. 63: 95-117.
doi: 10.1007/BF01064684
Flegr J. 2021: Toxoplasmosis is a risk factor for acquiring SARS-CoV-2 infection and a severe course of COVID-19 in the Czech and Slovak population: a preregistered exploratory internet cross-sectional study. Parasit. Vectors. 14: 508.
doi: 10.1186/s13071-021-05021-9
Flegr J. 2022a: Parasitic manipulation, or side-effects? The effects of past Toxoplasma and Borrelia infections on personality and cognitive performance of humans are not mediated by impaired health. Figshare, 6/2023. doi: https://doi.org/10.6084/m9.figshare.21151075.v1.
doi: 10.6084/m9.figshare.21151075.v1
Flegr J. 2022b: Adaptations, by-products, and spandrels. In: T.K. Shackelford (Ed.), Cambridge Handbook of Evolutionary Perspectives on Sexual Psychology: Volume 1, Foundations. Cambridge University Press, Cambridge, pp. 87-113.
doi: 10.1017/9781108943529.007
Flegr J., Escudero D.Q. 2016: Impaired health status and increased incidence of diseases in Toxoplasma-seropositive subjects - an explorative cross-sectional study. Parasitology 143: 1974-1989.
doi: 10.1017/S0031182016001785
Flegr J., Flegr P. 2021: Doing exploratory analysis in R with a package Explorer v. 1.0. Figshare, 6/2023.
doi: 10.1007/978-3-031-08956-5_386-1
Flegr J., Flegr P., Priplatova L. 2022: The effects of 105 biological, socioeconomic, behavioral, and environmental factors on the risk of SARS-CoV-2 infection and a severe course of COVID-19: a prospective, explorative cohort study. Biol. Methods Protoc. 7: bpac030.
doi: 10.1093/biomethods/bpac030
Flegr J., Guenter W., Bielinski M., Deptula A., Zalas-Wiecek P., Piskunowicz M., Szwed K., Buciński A., Gospodarek E., Borkowska A. 2012a: Toxoplasma gondii infection affects cognitive function - corrigendum. Folia Parasitol. 59: 253.
doi: 10.14411/fp.2012.035
Flegr J., Hampl R., Černochová D., Preiss M., Bičíková M., Sieger L., Příplatová L., Kaňková S., Klose J. 2012b: The relation of cortisol and sex hormone levels to results of psychological, performance, IQ and memory tests in military men and women. Neuro Endocrinol. Lett. 33: 224-235.
Flegr J., Havlíček J. 1999: Changes in the personality profile of young women with latent toxoplasmosis. Folia Parasitol. 46: 22-28.
Flegr J., Horáček J. 2017: Toxoplasma-infected subjects report an obsessive-compulsive disorder diagnosis more often and score higher in obsessive-compulsive inventory. Eur. Psychiatry 40: 82-87.
doi: 10.1016/j.eurpsy.2016.09.001
Flegr J., Horáček J. 2018: Toxoplasmosis, but not borreliosis, is associated with psychiatric disorders and symptoms. Schizophr. Res. 197: 603-604.
doi: 10.1016/j.schres.2018.02.008
Flegr J., Hrdý I. 1994: Influence of chronic toxoplasmosis on some human personality factors. Folia Parasitol. 41: 122-126.
Flegr J., Latifi A. 2023: The lasting legacy of covid-19: exploring the long-term effects of infection, disease severity, and vaccination on health and cognitive function. Biol. Methods Protoc. (in press).
doi: 10.1101/2023.04.12.23288455
Flegr J., Lenochová P., Hodný Z., Vondrová M. 2011: Fatal attraction phenomenon in humans: cat odour attractiveness increased for Toxoplasma-infected men while decreased for infected women. PloS Negl. Trop. Dis. 5: e1389.
doi: 10.1371/journal.pntd.0001389
Flegr J., Milinski M., Kankova S., Hula M., Hlavacova J., Sykorova K. 2018: Latent toxoplasmosis and olfactory functions of Rh positive and Rh negative subjects. PLoS One 13: e0209773.
doi: 10.1371/journal.pone.0209773
Flegr J., Prandota J., Sovickova M., Israili Z.H. 2014: Toxoplasmosis - a global threat. Correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS One 9: e90203.
doi: 10.1371/journal.pone.0090203
Flegr J., Preiss M., Klose J. 2013: Toxoplasmosis-associated difference in intelligence and personality in men depends on their Rhesus blood group but not ABO blood group. PLoS One 8: e61272.
doi: 10.1371/journal.pone.0061272
Flegr J., Příplatová L., Hlaváčová J., Šebánková B., Žďárský E., Kaňková Š. 2021: The importance of being heterozygote: effects of RHD-genotype-sex interaction on the physical and mental health of a non-clinical population. Sci. Rep. 11: 21960.
doi: 10.1038/s41598-021-00977-1
Flegr J., Stříž I. 2011: Potential immunomodulatory effects of latent toxoplasmosis in humans. BMC Infect. Dis. 11: 274.
doi: 10.1186/1471-2334-11-274
Flegr J., Zitkova S., Kodym P., Frynta, D. 1996: Induction of changes in human behaviour by the parasitic protozoan Toxoplasma gondii. Parasitology 113: 49-54.
doi: 10.1017/S0031182000066269
Gale S.D., Erickson L.D., Thacker E.L., Mitchell E.L., Brown B.L., Hedges D.W. 2020: Toxoplasma gondii seropositivity and serointensity and cognitive function in adults. PloS Negl. Trop. Dis. 14: e0008733.
doi: 10.1371/journal.pntd.0008733
Galuci M. 2021: PATHj: jamovi Path Analysis. (Computer software). Retrieved from https://pathj.github.io/, 11/2022.
Gosling S.D., Rentfrow P.J., Swann W.B. 2003: A very brief measure of the Big-Five personality domains. J. Res. Pers. 37: 504-528.
doi: 10.1016/S0092-6566(03)00046-1
Grabe H.J., Spitzer C., Ludemann J., Guertler L., Kramer A., John U., Freyberger H.J., Volzke H. 2008: No association of seropositivity for anti-Borrelia IgG antibody with mental and physical complaints. Nord. J. Psychiatr. 62: 386-391.
doi: 10.1080/08039480801984230
de Haan L., Sutterland A.L., Schotborgh J.V., Schirmbeck F., de Haan L. 2021: Association of Toxoplasma gondii seropositivity with cognitive function in healthy people: a systematic review and meta-analysis. JAMA Psychiatry 78: 1103-1112.
doi: 10.1001/jamapsychiatry.2021.1590
Halperin J.J. 2014: Lyme disease: neurology, neurobiology, and behavior. Clin. Infect. Dis. 58: 1267-1272.
doi: 10.1093/cid/ciu106
Havlíček J., Gašová Z., Smith A.P., Zvára K., Flegr J. 2001: Decrease of psychomotor performance in subjects with latent 'asymptomatic' toxoplasmosis. Parasitology 122: 515-520.
doi: 10.1017/S0031182001007624
Hernández-Ruiz V., Edjolo A., Roubaud-Baudron C., Jaulhac B., Avila-Funes J.A., Dartigues J.F., Amieva H., Pérès K. 2020: Association of seropositivity to Borrelia burgdorferi with the risk of neuropsychiatric disorders and functional decline in older adults: the aging multidisciplinary investigation study. JAMA Neurol. 77: 210-214.
doi: 10.1001/jamaneurol.2019.3292
Hodková H., Kodym P., Flegr J. 2007a: Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism? Parasitology 134: 1329-1337.
doi: 10.1017/S0031182007002673
Hodková H., Kolbeková P., Skallová A., Lindová J., Flegr J. 2007b: Higher perceived dominance in Toxoplasma infected men a new evidence for role of increased level of testosterone in toxoplasmosis-associated changes in human behavior. Neuro Endocrinol. Lett. 28: 110-114.
Hrdá Š., Votýpka J., Kodym P., Flegr J. 2000: Transient nature of Toxoplasma gondii-induced behavioral changes in mice. J. Parasitol. 86: 657-663.
doi: 10.1645/0022-3395(2000)086[0657:TNOTGI]2.0.CO;2
Hündersen F., Forst S., Kasten E. 2021: Neuropsychiatric and psychological symptoms in patients with Lyme disease: a study of 252 patients. Healthcare 9: 733.
doi: 10.3390/healthcare9060733
Jamovi 2021: The jamovi project. version 2.2. (Computer software) Retrieved from https://www.jamovi.org, 11/2022.
Jones D.N., Paulhus D.L. 2014: Introducing the short Dark Triad (SD3): a brief measure of dark personality traits. Assessment. 21: 28-41.
doi: 10.1177/1073191113514105
Kalish R.A., McHugh G., Granquist J., Shea B., Ruthazer R., Steere A.C. 2001: Persistence of immunoglobulin M or immunoglobulin G antibody responses to Borrelia burgdorferi 10-20 years after active Lyme disease. Clin. Infect. Dis. 33: 780-785.
doi: 10.1086/322669
Kaňková Š., Holáň V., Zajícová A., Kodym P., Flegr J. 2010: Modulation of immunity in mice with latent toxoplasmosis - the experimental support for the immunosupression hypothesis of Toxoplasma-induced changes in reproduction of mice and humans. Parasitol. Res. 107: 1421-1427.
doi: 10.1007/s00436-010-2013-9
Kodym P., Machala L., Roháčová H., Širocká B., Malý M. 2007: Evaluation of a commercial IgE ELISA in comparison with IgA and IgM ELISAs, IgG avidity assay and complement fixation for the diagnosis of acute toxoplasmosis. Clin. Microbiol. Infect. 13: 40-47.
doi: 10.1111/j.1469-0691.2006.01564.x
Kopecky R., Příplatová L., Boschetti S., Talmont-Kaminski K., Flegr J. 2022: Le Petit Machiavellian Prince: effects of latent toxoplasmosis on political beliefs and values. Evol. Psychol. 20: 13.
doi: 10.1177/14747049221112657
Kupfer T.R., Le A.T.D. 2018: Disgusting clusters: trypophobia as an overgeneralised disease avoidance response. Cogn. Emot. 32: 729-741.
doi: 10.1080/02699931.2017.1345721
Latifi A., Flegr J. 2023: Is recovery just the beginning? Persistent symptoms and health and performance deterioration in post-COVID-19, non-hospitalised university students - a cross-sectional study. Biol. Methods Protoc. (in press).
doi: 10.1101/2023.10.20.23297203
Lindová J., Kuběna A.A., Šturcová A., Křivohlavá R., Novotná M., Rubešová A., Havlíček J., Kodym P., Flegr J. 2010: Pattern of money allocation in experimental games supports the stress hypothesis of gender differences in Toxoplasma gondii-induced behavioural changes. Folia Parasitol. 57: 136-142.
doi: 10.14411/fp.2010.017
Lindová J., Příplatová L., Flegr J. 2012: Higher extraversion and lower conscientiousness in humans infected with Toxoplasma. Eur. J. Pers. 26: 285-291.
doi: 10.1002/per.838
Lorenz A.R., Libarkin J.C., Ording G.J. 2014: Disgust in response to some arthropods aligns with disgust provoked by pathogens. Glob. Ecol. Conserv. 2: 248-254.
doi: 10.1016/j.gecco.2014.09.012
Luft B.J., Remington J.S. 1992: Toxoplasmic encephalitis in AIDS. Clin. Infect. Dis. 15: 211-222.
doi: 10.1093/clinids/15.2.211
Makara-Studzinska M., Rolla-Szczepanska R., Urbanska A., Nowakowska-Domagala K., Stecz P. 2017: Anxiety and depression in patients infected with Borrelia burgdorferi. Eur. J. Psychiat. 31: 165-171.
doi: 10.1016/j.ejpsy.2017.09.003
Marvel C.L., Alm K.H., Bhattacharya D., Rebman A.W., Bakker A., Morgan O.P., Creighton J.A., Kozero E.A., Venkatesan A., Nadkarni P.A., Aucott J.N. 2022: A multimodal neuroimaging study of brain abnormalities and clinical correlates in post treatment Lyme disease. PLoS One 17: e0271425.
doi: 10.1371/journal.pone.0271425
McAuliffe P., Brassard M.R., Fallon B. 2008: Memory and executive functions in adolescents with posttreatment Lyme disease. Appl. Neuropsychol. 15: 208-219.
doi: 10.1080/09084280802324473
Meili R. 1961: Lehrbuch der Psychologischen Diagnostik. Verlag Hans Huber, Bern, 476 pp.
Mejzlíková T., Preiss M., Maliňáková J., Raisová M., Bolceková E. 2018: [Czech validation study of the Short Dark Triad Scale (SD3).] Aplikovaná Psychologie 5: 255-270. (In Czech.)
Mendy A., Vieira E.R., Albatineh A.N., Gasana J. 2015a: Immediate rather than delayed memory impairment in older adults with latent toxoplasmosis. Brain Behav. Immun. 45: 36-40.
doi: 10.1016/j.bbi.2014.12.006
Mendy A., Vieira E.R., Albatineh A.N., Gasana J. 2015b: Toxoplasma gondii seropositivity and cognitive functions in school-aged children. Parasitology 142: 1221-1227.
doi: 10.1017/S0031182015000505
Moore J. 2002: Parasites and the Behavior of Animals. Oxford University Press, Oxford, 338 pp.
doi: 10.1093/oso/9780195084412.001.0001
Oksi J., Kalimo H., Marttila R.J., Marjamaki M., Sonninen P., Nikoskelainen J., Viljanen M.K. 1996: Inflammatory brain changes in Lyme borreliosis: a report on three patients and review of literature. Brain 119: 2143-2154.
doi: 10.1093/brain/119.6.2143
Otis A.S. 1954: Otis Quick-Scoring Mental Ability Test, New Edition. Word Book Co., Tarrytown-on-Hudson, NY, 48 pp.
Poirotte C., Kappeler P.M., Ngoubangoye B., Bourgeois S., Moussodji M., Charpentier M.J.E. 2016: Morbid attraction to leopard urine in Toxoplasma-infected chimpanzees. Curr. Biol. 26: R98-R99.
doi: 10.1016/j.cub.2015.12.020
Robert-Gangneux F., Darde M.L. 2012: Epidemiology of and diagnostic strategies for toxoplasmosis. Clin. Microbiol. Rev. 25: 264-296.
doi: 10.1128/CMR.05013-11
Sapi E., Kasliwala R.S., Ismail H., Torres J.P., Oldakowski M., Markland S., Gaur G., Melillo A., Eisendle K., Liegner K. B., Libien, J., Goldman J.E. 2019: The long-term persistence of Borrelia burgdorferi antigens and DNA in the tissues of a patient with Lyme disease. Antibiotics 8: 183.
doi: 10.3390/antibiotics8040183
Scotti C., Webber M.L. 1995: Late-stage neuropsychiatric Lyme borreliosis differential diagnosis and treatment. Psychosomatics 36: 295-300.
doi: 10.1016/S0033-3182(95)71669-3
Shaw J.C., Korzan,W.J., Carpenter R.E., Kuris A.M., Lafferty K.D., Summers C.H., Overli O. 2009: Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc. Biol. Sci. 276: 1137-1146.
doi: 10.1098/rspb.2008.1597
Sroka J., Szymanska J., Wojcik-Fatla A. 2009: The occurrence of Toxoplasma gondii and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from east Poland with the use of PCR. Ann. Agric. Environ. Med. 16: 313-319.
Sutterland A., Fond G., Kuin A., Koeter M., Lutter R., Van Gool T., Yolken R., Szoke A., Leboyer M., De Haan L. 2015: Transdiagnostic exploration of the association of Toxoplasma gondii with psychiatric disorders. A systematic review and meta analysis. Eur. Psychiat. 30: 70.
doi: 10.1016/S0924-9338(15)30059-6
Sýkorová K., Flegr J. 2021: Faster life history strategy manifests itself by lower age at menarche, higher sexual desire, and earlier reproduction in people with worse health. Sci. Rep. 11: 11254.
doi: 10.1038/s41598-021-90579-8
Tetens M.M., Haahr R., Dessau R.B., Krogfelt K.A., Bodilsen J., Andersen N.S., Moller J.K., Roed C., Christiansen C.B., Ellermann-Eriksen S., Bangsborg J.M., Hansen K., Andersen C.O., Lebech A.M., Obel N., Omland L.H. 2021: Assessment of the risk of psychiatric disorders, use of psychiatric hospitals, and receipt of psychiatric medication among patients with Lyme neuroborreliosis in Denmark. JAMA Psychiatry 78: 177-186.
doi: 10.1001/jamapsychiatry.2020.2915
Torrey E.F., Bartko J.J., Yolken R.H. 2012: Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophr. Bull. 38: 642-647.
doi: 10.1093/schbul/sbs043
Tybur J.M., Lieberman D.L., Griskevicius V. 2009: Microbes, mating, and morality: individual differences in three functional domains of disgust. J. Pers. Soc. Psychol. 97: 103-122.
pubmed: 19586243 doi: 10.1037/a0015474
Vyas A., Kim S.K., Giacomini N., Boothroyd J.C., Sapolsky R.M. 2007: Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. USA 104: 6442-6447.
pubmed: 17404235 doi: 10.1073/pnas.0608310104
Wiener R.C., Waters C., Bhandari R. 2020: The association of Toxoplasma gondii IgG and cognitive function scores: NHANES 2013-2014. Parasitol. Int. 78: 102123.
pubmed: 32416258 doi: 10.1016/j.parint.2020.102123
Woke P.A., Jacobs L., Jones F.E., Melton M.L. 1953: Experimental results on possible arthropod transmission of toxoplasmosis. J. Parasitol. 39: 523-532.
doi: 10.2307/3273853
Wyman C.P., Gale S.D., Hedges-Muncy A., Erickson L.D., Wilson E., Hedges D.W. 2017: Association between Toxoplasma gondii seropositivity and memory function in nondemented older adults. Neurobiol. Aging 53: 76-82.
pubmed: 28235681 doi: 10.1016/j.neurobiolaging.2017.01.018

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