Advances in the mechanism underlying the interaction of Toxoplasma gondii and nematodes co-infections

doi:10.12140/j.issn.1000-7423.2025.04.017

Abstract

Abstract:

Parasitic co-infection is common in the natural world, which may affect both host immune responses and the pathogenesis of parasites. Protozoa and helminths are found to induce different immune responses, and protozoa and helminths co-infections may affect host immune response to these parasites and the outcomes of infections. Toxoplasma gondii is a neurotropic protozoan parasite causing persistent subclinical neuroinflammations, which is associated with psychiatric and neurodegenerative diseases, as well as other diseases. However, there has been limited knowledge on the mechanisms underlying the interaction of T. gondii and nematodes co-infections until now. This review provides an overview of the interactions and regulatory mechanisms of T. gondii co-infections with Toxocara spp., Trichinella spiralis, Heligmosomoides spp. and Nippostrongylus brasiliensis in human or animal hosts.

Key words: Toxoplasma gondii, Nematodes, Co-infection, Interaction, Mechanism

CLC Number:

R382.5

LV Fangli, LIN Xincheng. Advances in the mechanism underlying the interaction of Toxoplasma gondii and nematodes co-infections[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2025, 43(4): 562-566.

References 39

[1]	Soares Magalh?es RJ, Biritwum NK, Gyapong JO, et al. Mapping helminth co-infection and co-intensity: Geostatistical prediction in Ghana[J]. PLoS Negl Trop Dis, 2011, 5(6): e1200.
[2]	Clark NJ, Owada K, Ruberanziza E, et al. Parasite associations predict infection risk: Incorporating co-infections in predictive models for neglected tropical diseases[J]. Parasit Vectors, 2020, 13(1): 138.
[3]	Wang ZD, Wang SC, Liu HH, et al. Prevalence and burden of Toxoplasma gondii infection in HIV-infected people: A systematic review and meta-analysis[J]. Lancet HIV, 2017, 4(4): e177.e188.
[4]	Piazzesi A, Putignani L. Impact of helminth-microbiome interactions on childhood health and development-a clinical perspective[J]. Parasite Immunol, 2023, 45(4): e12949.
[5]	Sorobetea D, Svensson-Frej M, Grencis R. Immunity to gastrointestinal nematode infections[J]. Mucosal Immunol, 2018, 11(2): 304-315.
[6]	Fadaei T, Saki J, Arjmand R, et al. Toxoplasma gondii and Toxocara spp. contamination in university area[J]. Ann Parasitol, 2024, 70(2): 101-111.
[7]	Jones JL, Kruszon-Moran D, Won K, et al. Toxoplasma gondii and Toxocara spp. co-infection[J]. Am J Trop Med Hyg, 2008, 78(1): 35-39.
[8]	Montoya J, Liesenfeld O. Toxoplasmosis[J]. Lancet, 2004, 363(9425): 1965-1976.
[9]	Ma GX, Holland CV, Wang T, et al. Human toxocariasis[J]. Lancet Infect Dis, 2018, 18(1): e14.e24.
[10]	Schoenardie ER, Scaini CJ, Pepe MS, et al. Vertical transmission of Toxocara canis in successive generations of mice[J]. Rev Bras Parasitol Vet, 2013, 22(4): 623-626.
[11]	Santos PC, Telmo PL, Lehmann LM, et al. Risk and other factors associated with toxoplasmosis and toxocariasis in pregnant women from southern Brazil[J]. J Helminthol, 2017, 91(5): 534-538.
[12]	Cabral Monica T, Evers F, de Souza Lima Nino B, et al. Socioeconomic factors associated with infection by Toxoplasma gondii and Toxocara canis in children[J]. Transbound Emerg Dis, 2022, 69(3): 1589-1595.
[13]	Pacheco-Ortega GA, Chan-Pérez JI, Ortega-Pacheco A, et al. Screening of zoonotic parasites in playground sandboxes of public parks from subtropical Mexico[J]. J Parasitol Res, 2019, 2019: 7409076.
[14]	Poulin R. The evolution of parasite manipulation of host behaviour: A theoretical analysis[J]. Parasitology, 1994, 109 Suppl: S109.S118.
[15]	Holland CV, Cox DM. Toxocara in the mouse: A model for parasite-altered host behaviour?[J]. J Helminthol, 2001, 75(2): 125-135.
[16]	Webster JP. Rats, cats, people and parasites: The impact of latent toxoplasmosis on behaviour[J]. Microbes Infect, 2001, 3(12): 1037-1045.
[17]	Dubey JP. Tissue cyst tropism in Toxoplasma gondii: A comparison of tissue cyst formation in organs of cats, and rodents fed oocysts[J]. Parasitology, 1997, 115 (Pt 1): 15-20.
[18]	Boillat M, Hammoudi PM, Dogga SK, et al. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasma gondii[J]. Cell Rep, 2020, 30(2): 320-334. e6.
[19]	Berdoy M, Webster JP, Macdonald DW. Fatal attraction in rats infected with Toxoplasma gondii[J]. Proc Biol Sci, 2000, 267(1452): 1591-1594.
[20]	Abdulai-Saiku S, Tong WH, Vyas A. Behavioral manipulation by Toxoplasma gondii: Does brain residence matter?[J]. Trends Parasitol, 2021, 37(5): 381-390.
[21]	Cox DM, Holland CV. The relationship between numbers of larvae recovered from the brain of Toxocara canis-infected mice and social behaviour and anxiety in the host[J]. Parasitology, 1998, 116 ( Pt 6): 579-594.
[22]	Holland CV, Hamilton CM. The significance of cerebral toxocariasis: A model system for exploring the link between brain involvement, behaviour and the immune response[J]. J Exp Biol, 2013, 216(Pt 1): 78-83.
[23]	Santos SV, Moura JVL, Lescano SAZ, et al. Behavioural changes and muscle strength in Rattus norvegicus experimentally infected with Toxocara cati and T. canis[J]. J Helminthol, 2015, 89(4): 465-470.
[24]	Corrêa FM, Chieffi PP, Lescano SAZ, et al. Behavioral and memory changes in Mus musculus coinfected by Toxocara canis and Toxoplasma gondii[J]. Rev Inst Med Trop Sao Paulo, 2014, 56(4): 353-356.
[25]	Witting PA. Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice[J]. Z Parasitenkd, 1979, 61(1): 29-51.
[26]	Lescano SA, Nakhle MC, Ribeiro MC. IgG antibody responses in mice coinfected with Toxocara canis and other helminths or protozoan parasites[J]. Rev Inst Med Trop Sao Paulo, 2012, 54(3): 145-152.
[27]	Queiroz ML, Viel TA, Papa CHG, et al. Behavioral changes in Rattus norvegicus coinfected by Toxocara canis and Toxoplasma gondii[J]. Rev Inst Med Trop Sao Paulo, 2013, 55(1): 51-53.
[28]	Thomas F, Adamo S, Moore J. Parasitic manipulation: Where are we and where should we go?[J]. Behav Processes, 2005, 68(3): 185-199.
[29]	Li R, Zhang B, Chen C. Comparison of structures and inhibition activities of serine protease inhibitors of Trichinella spiralis and Trichinella pseudospiralis[J]. Cell Biosci, 2025, 15(1): 35.
[30]	Saad AE, Ashour DS, Rashad E. Immunomodulatory effects of chronic trichinellosis on Toxoplasma gondii RH virulent strain in experimental rats[J]. Pathog Glob Health, 2023, 117(4): 417-434.
[31]	Bokken GCAM, van Eerden E, Opsteegh M, et al. Specific serum antibody responses following a Toxoplasma gondii and Trichinella spiralis co-infection in swine[J]. Vet Parasitol, 2012, 184(2/3/4): 126-132.
[32]	Maizels RM, Hewitson JP, Murray J, et al. Immune modulation and modulators in Heligmosomoides polygyrus infection[J]. Exp Parasitol, 2012, 132(1): 76-89.
[33]	Szabo EK, Bowhay C, Forrester E, et al. Heligmosomoides bakeri and Toxoplasma gondii co-infection leads to increased mortality associated with changes in immune resistance in the lymphoid compartment and disease pathology[J]. PLoS One, 2024, 19(7): e0292408.
[34]	Ahmed N, French T, Rausch S, et al. Toxoplasma co-infection prevents Th2 differentiation and leads to a helminth-specific Th1 response[J]. Front Cell Infect Microbiol, 2017, 7: 341.
[35]	Rovira-Diaz E, El-Naccache DW, Reyes J, et al. The impact of helminth coinfection on innate and adaptive immune resistance and disease tolerance during toxoplasmosis[J]. J Immunol, 2022, 209(11): 2160-2171.
[36]	French T, Düsedau HP, Steffen J, et al. Neuronal impairment following chronic Toxoplasma gondii infection is aggravated by intestinal nematode challenge in an IFN-γ-dependent manner[J]. J Neuroinflammation, 2019, 16(1): 159.
[37]	Marple A, Wu WH, Shah S, et al. Cutting edge: Helminth coinfection blocks effector differentiation of CD8 T cells through alternate host Th2- and IL-10-mediated responses[J]. J Immunol, 2017, 198(2): 634-639.
[38]	Camberis M, Le Gros G, Urban Jr J. Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus[J]. Curr Protoc Immunol, 2003, 55: 19.12. 1-19.12.27.
[39]	Liesenfeld O, Dunay IR, Erb KJ. Infection with Toxoplasma gondii reduces established and developing Th2 responses induced by Nippostrongylus brasiliensis infection[J]. Infect Immun, 2004, 72(7): 3812-3822.