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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Animal Parasitic Diseases Laboratory » Research » Publications at this Location » Publication #306694

Title: Immune and inflammatory responses in pigs infected with Trichuris suis and Oesophagostomum dentatum

item ANDREASEN, ANNETTE - University Of Copenhagen
item PETERSEN, HEIDI - University Of Copenhagen
item KRINGEL, HELENE - University Of Copenhagen
item IBURG, TINE - Danish Technical University
item SKOVGAARD, KERSTIN - Danish Technical University
item Dawson, Harry
item Urban, Joseph
item THAMSBORG, STIG - University Of Copenhagen

Submitted to: Veterinary Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/15/2014
Publication Date: 1/30/2015
Citation: Andreasen, A., Petersen, H., Kringel, H., Iburg, T., Skovgaard, K., Dawson, H.D., Urban Jr, J.F., Thamsborg, S. 2015. Immune and inflammatory responses in pigs infected with Trichuris suis and Oesophagostomum dentatum. Veterinary Parasitology. 207(3-4):249-258.

Interpretive Summary: The aim of the present study was to investigate how a concurrent infection with Trichuris suis and Oesophogostomum in pigs influences the parasite induced immune and inflammatory host responses as compared to mono-species infected animals. Experimental studies on parasite population dynamics and host immune responses in helminth infections often focus on one species, even though it is the rule rather than the exception for animals and humans to be naturally infected with two or more helminth species. The population dynamics in cooccurring experimental helminth infections are complex, but basically there are three different possible outcomes: Antagonistic interaction (negative effect on populations of one or both species), synergistic interaction (positive effect on one or both species) or no interaction (neutral effect) between the species. The outcome may depend upon a variety of factors, such as the host, the phylogenetical and/or ecological relationship (sharing of habitat/resources) between the helminths, the timing of infections (sequential or simultaneous) and the infection doses of the helminths. The mechanisms behind helminth interactions can essentially be explained by means of altered ecology (habitat/resource use) and/or immune responses of the host. It is now possible to investigate interactions in host immune responses to specific helminth combinations in co-existence using a number of standard and molecular assays of host/parasite interaction. To date little is known about the outcome of a mixed infection of Oesophagostomum spp. and T. suis but we hypothesized an antagonistic interaction, i.e. a suppression of Oesophagostomum spp. when co-infected with T. suis. The results showed that T. suis induced a strong circulating antibody and localized cytokine response to infection that could explain a reduction in number and fecundity of Oesophagostomum spp during a coinfection.

Technical Abstract: The aim of the present study was to investigate parasite induced immune responses in pigs co-infected with Trichuris suis and Oesophagostomum dentatum as compared to mono-species infected pigs. T. suis is known to elicit a strong immune response leading to rapid expulsion, and a strong antagonistic effect on O. dentatum populations has been observed in co-infected pigs. Forty-eight helminth naïve pigs were allocated into 4 groups in a 2-factorial design. Two groups were trickle inoculated with either 10 T. suis eggs/kg/day (Group T) or 20 O. dentatum L3/kg/day (Group O). Group OT was infected with same levels of both T. suis and O. dentatum (Group OT) and Group C remained uninfected. In each group, six pigs were necropsied after 35 days and the remaining pigs after 71 days. Parasite E/S-antigen specific serum antibodies were quantified by an in-direct ELISA regularly. qPCR was used to measure the expression of immune function related genes in the mucosa of proximal colon and the draining lymph node. Highly significant interactions were identified for O. dentatum specific IgG1 (p<0.0001) and IgG2 (p<0.0006) antibodies with a remarkable 2-fold higher antibody response in group OT pigs as compared to group O. These findings indicated that T. suis enhanced the antibody response against O. dentatum in Group OT. The gene expression data confirmed a strong Type 2 response to T. suis (e. g. marked increase in IL-13, ARG1 and CCL11) and clearly weaker in amplitude and delayed onset response to O. dentatum in the single infected group. Statistical interactions were found between the two nematodes with regard to several cytokines, e.g. the increase in IL-13 observed in Group T was absent in Group OT (p=0.06, PCM, 35 and 71 p.i.). Some of these immune response-related interactions may support, or even partially explain, the observed interactions between the two worm populations in co-infected pigs.