Chronic Intestinal Nematode Infection Exacerbates ExperimentalSchistosoma mansoniInfection

Abstract

Mixed-parasite infections are common in many parts of the world, but little is known of the effects of concomitant parasite infections on the immune response or on disease progression. We have investigated the in vivo effects of a chronic gastrointestinal nematode infection on the infectivity and development of the immune response against the common trematode helminth Schistosoma mansoni. The data show that mice carrying an established chronic Trichuris muris infection and coinfected with S. mansoni, had significantly higher S. mansoni worm burdens than mice without coinfection. The increase in S. mansoni worm burden was accompanied by a higher egg burden in the liver. Kinetic analysis of S. mansoni establishment indicate reduced trapping of S. mansoni larvae during skin-to-lung migration, with T. muris-induced alterations in lung cytokine expression and inflammatory foci surrounding lung-stage schistosomula, suggesting that the immunomodulatory effects of chronic T. muris infection elicited at the gut mucosal surface extend to other organs and perhaps specifically to other mucosal surfaces. The data show that a preexisting chronic gastrointestinal nematode infection facilitates the survival and migration of S. mansoni schistosomula to the portal system, and as a result, increases the egg burden and associated pathology of S. mansoni infection.Helminth infections are among the most common infections of humans (2,7,26). Helminth infections are characteristically chronic in nature, and in order to achieve such long-lasting infections, these parasites have developed sophisticated survival strategies such as secretion of immunomodulatory substances and/or the induction of regulatory immune responses (35). These immunomodulatory activities may alter immune responsiveness to third party antigens such as vaccines (9, 10, 18, 42) and concurrent infections (reviewed in references 4 and 27). Intriguingly, recent studies have also demonstrated that the immunomodulatory effects of helminth infections may have beneficial effects, such as controlling allergy and inflammatory diseases (19,53).Individuals living in areas where helminths are endemic often carry more than one species of worm infection; egg output for an individual helminth species is often higher in individuals carrying mixed infections than in individuals carrying singlespecies infections (3,5,20,38,45), which may reflect higher intensities of infection and so a higher risk of morbidity. Geographical and environmental factors are known to be of significance in facilitating this type of polyparasitism: for example, similarities in the transmission pathways for certain soil-transmitted nematodes are likely to account for some of the observed associations. However, significant associations have also been demonstrated between helminth infections that do not share obvious transmission pathways and some of these associations are not explained solely by household or environmental effects (20). Furthermore, the intensity of helminth infections alters the risk of multipl...

The Influence of Parasite Infections on Host Immunity to Co-infection With Other Pathogens

“…A chronic Trichuris muris infection within the large intestine enhanced the survival and migration of S. mansoni schistosomula to the portal system. Consequently, schistosome worm and egg burdens and associated pathology were enhanced when compared to mice infected with S. mansoni alone ( 34 ). This suggests that the immunomodulatory effects elicited in the mucosa of the large intestine to enable the gastrointestinal helminth to establish chronic infection can extend to other host tissues.…”

Chronic whipworm infection exacerbates Schistosoma mansoni egg-induced hepatopathology in non-human primates

“…There are insufficient studies on the interactions of trichuriasis and schistosomiasis, specifically on the influence of co-infection on Schistosoma mansoni egg-induced hepatopathology. Others have found that concomitant infections of Schistosoma japonicum and Trichuris significantly increased the odds of anemia in children [4] and that mice with established chronic Trichuris muris infection and challenged with S. mansoni developed significantly higher S. mansoni worm burden and egg and granuloma burden in the liver [5]. To prepare for deployment of interventions such as vaccines against schistosomiasis [6], it is critical to understand the interactions between potential confounding factors that will be present in endemic areas, such as polyparasitism.…”

Order of Inoculation during Heligmosomoides bakeri and Hymenolepis microstoma Coinfection Alters Parasite Life History and Host Responses

“…The dynamics of coinfection are clearly multi-faceted and not surprisingly the documented outcomes of these relationships vary such that infection with one parasite species may enhance (e.g., [ 3 , 4 , 5 ]), diminish (e.g., [ 6 , 7 ]), or not affect (e.g., [ 8 , 9 ]) the establishment or survival of another parasite species. How parasite species respond to the presence of each other varies tremendously [ 10 ] and may be influenced by the particular species involved, location of the parasites in the host, duration of coinfection [ 11 ], strain differences within a parasite species [ 12 ], or which parasite infects the host first [ 13 , 14 ].…”