Abstract
BackgroundAlthough Plasmodium parasites and intestinal helminths share common endemic areas, the mechanisms of these co-infections on the host immune response remain not fully understood. Liver involvement in severe Plasmodium falciparum infections is a significant cause of morbidity and mortality. However, the effect of pre-existing Trichinella spiralis infection on the immune response and liver immune-pathogenesis in P. berghei ANKA (PbANKA)-infected mice needs to be elucidated.MethodsOutbred Kunming mice were infected with T. spiralis and 9 days later were challenged with P. berghei ANKA (PbANKA), and the investigation occurred at 13 days after co-infection.ResultsCompared with PbANKA-mono-infected mice, T. spiralis + PbANKA-co-infected mice had similar survival rate but lower PbANKA parasitaemia; however, there were more severe hepatosplenomegaly, increased liver and spleen indexes, and increased liver pathology observed by hematoxylin and eosin staining; higher expression levels of galectin (Gal)-1, Gal-3, CD68+ macrophages, and elastase-positive neutrophils measured by immunohistochemical staining; upregulated mRNA expression levels of Gal-1, Gal-3, cytokines (interferon-gamma (IFNγ) and interleukin (IL)-6), and M1 macrophage polarization marker (inducible nitric oxide synthase (iNOS)) in the liver, and increased expression levels of Gal-1, IFNγ, IL-6, eosinophil cationic protein, eosinophil protein X, and M1 (IL-1β and iNOS) and M2 (Ym1) macrophage polarization markers in the spleen of co-infected mice detected by using quantitative real-time reverse transcription polymerase chain reaction (qRT-PCR). In vitro study showed that compared with PbANKA-mono-infected mice, there were significantly increased expression levels of Gal-1, Gal-3, IL-6, IL-1β, and iNOS in the peritoneal macrophage isolated from co-infected mice detected by using qRT-PCR. Correlation analysis revealed significant positive correlations between Gal-3 and IL-1β in the peritoneal macrophages isolated from PbANKA-mono-infected mice, between Gal-3 and IFNγ in the spleen of co-infected mice, and between Gal-1 and Ym1 in the peritoneal macrophages isolated from co-infected mice.ConclusionsOur data indicate that pre-existing infection of T. spiralis may suppress P. berghei parasitaemia and aggravate malaria-induced liver pathology through stimulating Gal-1 and Gal-3 expression, activating macrophages, neutrophils, and eosinophils, and promoting mediator release and cytokine production.
Highlights
Plasmodium parasites and intestinal helminths share common endemic areas, the mechanisms of these co-infections on the host immune response remain not fully understood
Our data indicate that pre-existing infection of T. spiralis may suppress P. berghei parasitaemia and aggravate malaria-induced liver pathology through stimulating Gal-1 and Gal-3 expression, activating macrophages, neutrophils, and eosinophils, and promoting mediator release and cytokine production
Prior T. spiralis infection decreased parasitemia of P. berghei ANKA (PbANKA)‐infected mice without affecting overall survival To investigate whether prior T. spiralis infection alters the course of a subsequent malaria infection, we compared the changes in body weight, survival rate, and parasitemia of age-matched Kunming mice monoinfected with PbANKA or infected with T. spiralis and 9 days later challenged with PbANKA
Summary
Plasmodium parasites and intestinal helminths share common endemic areas, the mechanisms of these co-infections on the host immune response remain not fully understood. The manifestations of severe malaria often present clinically as cerebral malaria, pulmonary edema, acute kidney injury, hypoglycaemia, lactic acidosis, anemia, and liver involvement [1]. Malaria remains a serious public health issue in subSaharan region, while soil-transmitted helminths, such as Ascaris lumbricoides, Trichuris trichiura, and the hookworm species, infect more than a billion people worldwide [3], which have wide geographical overlap with malaria prevalent areas [4]. Mixed Plasmodium falciparum and P. vivax infections were found to be more frequent in A. lumbricoides-infected patients in Thailand, while infection with A. lumbricoides was associated with a dose-dependent effect on protection from cerebral malaria and acute renal failure [6]. It has been shown that heavy A. lumbricoides and T. trichiura infections were associated with high P. falciparum parasitaemia in a peri-urban community in Kwara State, Nigeria [10]
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