Generic placeholder image

Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry


ISSN (Print): 1871-5230
ISSN (Online): 1875-614X

Review Article

Human Toxocara Infection: Allergy and Immune Responses

Author(s): Mohammad Zibaei*, Zahra Shayesteh*, Najmeh Moradi and Saeed Bahadory

Volume 18, Issue 2, 2019

Page: [82 - 90] Pages: 9

DOI: 10.2174/1871523018666181210115840

Price: $65


Background: Toxocariasis is a cosmopolitan infection that occurs in various regions worldwide, more frequently in developing countries. Chronic infections with Toxocara species in humans are associated with the production of high levels of specific and non-specific antibodies of all isotypes and IgG subclasses and a cytokine response characterized by the production of Th2 cytokines including IL-4, IL-5 and IL-13 by Peripheral Blood Monocytes (PBMCs) and Leukocytes (PBLs) in whole blood cultures. Other Th2 effector responses are also prominent during infection, reflected by elevated numbers of peripheral blood eosinophils and increased expression of eosinophil degranulation products. The production of IFN-γ by PBMCs/PBLs stimulated with Toxocara-secreted proteins is not prominent in toxocariasis but IL-10 production may be increased in infected individuals. The relationship between Toxocara species with allergic reactions was reported in the recent century. Experimental and epidemiological investigations revealed that toxocariasis with this parasite led to the development of allergic symptoms, such as asthma. However, the findings are conflicting since in other investigations no association between these two immunopathologies has been reported.

Conclusion: The present review endeavours to summarize the data on Toxocara species and findings from studies on the relationship of toxocariasis with symptoms and signs of allergy. Furthermore, the mechanisms of immune responses and the factors associated between allergy and Toxocara infection are discussed.

Keywords: Allergy, asthma, immune response, toxocariasis, visceral larva migrans, leukocytes.

« Previous
Graphical Abstract
Despommier, D. Toxocariasis: Clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin. Microbiol. Rev., 2003, 16(2), 265-272.
Zibaei, M.; Sadjjadi, S.M.; Maraghi, S. The occurrence of Toxocara species in naturally infected broiler chickens revealed by molecular approaches. J. Helminthol., 2017, 91(5), 633-636.
Zibaei, M.; Sadjjadi, S.M. Trend of toxocariasis in Iran: A review on human and animal dimensions. Majallah-i Tahqiqat-i Dampizishki-i Iran, 2017, 18(4), 233-242.
Zibaei, M.; Sadjjadi, S.M.; Jahadi-Hosseini, S.H. Toxocara cati larvae in the eye of a child: A case report. Asian Pac. J. Trop. Biomed., 2014, 4(Suppl. 1), S53-S55.
Zibaei, M.; Sadjjadi, S.M.; Sarkari, B.; Uga, S. Evaluation of Toxocara cati excretory-secretory larval antigens in serodiagnosis of human toxocariasis. J. Clin. Lab. Anal., 2016, 30(3), 248-253.
Bartemes, K.R.; Kephart, G.M.; Fox, S.J.; Kita, H. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J. Allergy Clin. Immunol., 2014, 134(3), 671-678.
Kim, Y.M.; Kim, Y.S.; Jeon, S.G.; Kim, Y.K. Immunopathogenesis of allergic asthma: More than the Th2 hypothesis. Allergy Asthma Immunol. Res., 2013, 5(4), 189-196.
Pelaia, G.; Vatrella, A.; Busceti, M.T.; Gallelli, L.; Calabrese, C.; Terracciano, R.; Maselli, R. Cellular mechanisms underlying eosinophilic and neutrophilic airway inflammation in asthma. Mediators Inflamm., 2015, 2015879783
Loftus, P.A.; Wise, S.K. Epidemiology of asthma. Curr. Opin. Otolaryngol. Head Neck Surg., 2016, 24(3), 245-249.
Sitcharungsi, R.; Sirivichayakul, C. Allergic diseases and helminth infections. Pathog. Glob. Health, 2013, 107(3), 110-115.
Fialho, P.M.M.; Correa, C.R.S.; Lescano, S.Z.M. Asthma and seroconversion from Toxocara spp. infection: Which comes first? BioMed Res. Int., 2018, 20184280792
Feary, J.; Britton, J.; Leonardi-Bee, J. Atopy and current intestinal parasite infection: A systematic review and meta-analysis. Allergy, 2011, 66(4), 569-578.
Leonardi-Bee, J.; Pritchard, D.; Britton, J. Asthma and current intestinal parasite infection: Systematic review and meta-analysis. Am. J. Respir. Crit. Care Med., 2006, 174(5), 514-523.
Haileamlak, A.; Dagoye, D.; Williams, H.; Venn, A.J.; Hubbard, R.; Britton, J.; Lewis, S.A. Early life risk factors for atopic dermatitis in Ethiopian children. J. Allergy Clin. Immunol., 2005, 115(2), 370-376.
Lynch, N.R.; Hagel, I.; Perez, M.; Di Prisco, M.C.; Lopez, R.; Alvarez, N. Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J. Allergy Clin. Immunol., 1993, 92(3), 404-411.
Wördemann, M.; Diaz, R.J.; Heredia, L.M.; Collado Madurga, A.M.; Ruiz Espinosa, A.; Prado, R.C.; Millan, I.A.; Escobedo, A.; Rojas Rivero, L.; Gryseels, B.; Gorbea, M.B.; Polman, K. Association of atopy, asthma, allergic rhinoconjunctivitis, atopic dermatitis and intestinal helminth infections in Cuban children. Trop. Med. Int. Health, 2008, 13(2), 180-186.
Cooper, P.J. Interactions between helminth parasites and allergy. Curr. Opin. Allergy Clin. Immunol., 2009, 9(1), 29-37.
Erb, K.J. Can helminths or helminth-derived products be used in humans to prevent or treat allergic diseases? Trends Immunol., 2009, 30(2), 75-82.
van den Biggelaar, A.H.; Rodrigues, L.C.; van Ree, R.; van der Zee, J.S.; Hoeksma-Kruize, Y.C.; Souverijn, J.H.; Missinou, M.A.; Borrmann, S.; Kremsner, P.G.; Yazdanbakhsh, M. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J. Infect. Dis., 2004, 189(5), 892-900.
Hunninghake, G.M.; Soto-Quiros, M.E.; Avila, L.; Ly, N.P.; Liang, C.; Sylvia, J.S.; Klanderman, B.J.; Silverman, E.K.; Celedón, J.C. Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica. J. Allergy Clin. Immunol., 2007, 119(3), 654-661.
Anthony, R.M.; Rutitzky, L.I.; Urban, J.F., Jr; Stadecker, M.J.; Gause, W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol., 2007, 7(12), 975-987.
McSorley, H.J.; Maizels, R.M. Helminth infections and host immune regulation. Clin. Microbiol. Rev., 2012, 25(4), 585-608.
Aranzamendi, C.; Sofronic-Milosavljevic, L.; Pinelli, E. Helminths: Immunoregulation and inflammatory diseases which side are Trichinella spp. and Toxocara spp. on? J. Parasitol. Res., 2013, 2013329438
Gause, W.C.; Wynn, T.A.; Allen, J.E. Type 2 immunity and wound healing: Evolutionary refinement of adaptive immunity by helminths. Nat. Rev. Immunol., 2013, 13(8), 607-614.
Maizels, R.M.; Yazdanbakhsh, M. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat. Rev. Immunol., 2003, 3(9), 733-744.
Maizels, R.M. Toxocara canis: Molecular basis of immune recognition and evasion. Vet. Parasitol., 2013, 193(4), 365-374.
Pinelli, E.; Aranzamendi, C. Toxocara infection and its association with allergic manifestations. Endocr. Metab. Immune Disord. Drug Targets, 2012, 12(1), 33-44.
Cooper, P.J. Toxocara canis infection: An important and neglected environmental risk factor for asthma? Clin. Exp. Allergy, 2008, 38(4), 551-553.
Yasuda, K.; Muto, T.; Kawagoe, T.; Matsumoto, M.; Sasaki, Y.; Matsushita, K.; Taki, Y.; Futatsugi-Yumikura, S.; Tsutsui, H.; Ishii, K.J.; Yoshimoto, T.; Akira, S.; Nakanishi, K. Contribution of IL-33-activated type II innate lymphoid cells to pulmonary eosinophilia in intestinal nematode-infected mice. Proc. Natl. Acad. Sci. USA, 2012, 109(9), 3451-3456.
Nagaraj, S.H.; Harsha, H.C.; Reverter, A.; Colgrave, M.L.; Sharma, R.; Andronicos, N.; Hunt, P.; Menzies, M.; Lees, M.S.; Sekhar, N.R.; Pandey, A.; Ingham, A. Proteomic analysis of the abomasal mucosal response following infection by the nematode, Haemonchus contortus, in genetically resistant and susceptible sheep. J. Proteomics, 2012, 75(7), 2141-2152.
Price, A.E.; Liang, H.E.; Sullivan, B.M.; Reinhardt, R.L.; Eisley, C.J.; Erle, D.J.; Locksley, R.M. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA, 2010, 107(25), 11489-11494.
Voehringer, D. The role of basophils in helminth infection. Trends Parasitol., 2009, 25(12), 551-556.
Perrigoue, J.G.; Saenz, S.A.; Siracusa, M.C.; Allenspach, E.J.; Taylor, B.C.; Giacomin, P.R.; Nair, M.G.; Du, Y.; Zaph, C.; van Rooijen, N.; Comeau, M.R.; Pearce, E.J.; Laufer, T.M.; Artis, D. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nat. Immunol., 2009, 10(7), 697-705.
Holland, C.V.; Smith, H.V. Toxocara: The enigmatic parasite: CABI 2006.
Aalberse, R.; Koshte, V.; Clemens, J. Cross-reactions between vegetable foods, pollen and bee venom due to IgE antibodies to a ubiquitous carbohydrate determinant. Int. Arch. Allergy Immunol., 1981, 66, 259-260.
Dissous, C.; Grzych, J.M.; Capron, A. Schistosoma mansoni shares a protective oligosaccharide epitope with freshwater and marine snails. Nature, 1986, 323(6087), 443-445.
Grzych, J.M.; Dissous, C.; Capron, M.; Torres, S.; Lambert, P.H.; Capron, A. Schistosoma mansoni shares a protective carbohydrate epitope with keyhole limpet hemocyanin. J. Exp. Med., 1987, 165(3), 865-878.
van Die, I.; Gomord, V.; Kooyman, F.N.; van den Berg, T.K.; Cummings, R.D.; Vervelde, L. Core α1-3-fucose is a common modification of N-glycans in parasitic helminths and constitutes an important epitope for IgE from Haemonchus contortus infected sheep. FEBS Lett., 1999, 463(1-2), 189-193.
Lescano, S.A.Z.; Nakhle, M.C.; Ribeiro, M.C.S.; Chieffi, P.P. IgG antibody responses in mice coinfected with Toxocara canis and other helminths or protozoan parasites. Rev. Inst. Med. Trop. São Paulo, 2012, 54, 145-152.
Kuroda, E.; Yoshida, Y. En Shan, B.; Yamashita, U. Suppression of macrophage interleukin-12 and tumour necrosis factor-α production in mice infected with Toxocara canis. Parasite Immunol., 2001, 23(6), 305-311.
Torina, A.; Caracappa, S.; Barera, A.; Dieli, F.; Sireci, G.; Genchi, C.; Deplazes, P.; Salerno, A. Toxocara canis infection induces antigen-specific IL-10 and IFNgamma production in pregnant dogs and their puppies. Vet. Immunol. Immunopathol., 2005, 108(1-2), 247-251.
Fillaux, J.; Magnaval, J.F. Laboratory diagnosis of human toxocariasis. Vet. Parasitol., 2013, 193(4), 327-336.
Reiterová, K.; Tomasovicová, O.; Dubinský, P. Influence of maternal infection on offspring immune response in murine larval toxocariasis. Parasite Immunol., 2003, 25(7), 361-368.
Buijs, J.; Lokhorst, W.H.; Robinson, J.; Nijkamp, F.P. Toxocara canis-induced murine pulmonary inflammation: Analysis of cells and proteins in lung tissue and bronchoalveolar lavage fluid. Parasite Immunol., 1994, 16(1), 1-9.
Pinelli, E.; Withagen, C.; Fonville, M.; Verlaan, A.; Dormans, J.; van Loveren, H.; Nicoll, G.; Maizels, R.M.; van der Giessen, J. Persistent airway hyper-responsiveness and inflammation in Toxocara canis-infected BALB/c mice. Clin. Exp. Allergy, 2005, 35(6), 826-832.

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy