Co-infection: the outcome of Plasmodium infection differs according to the time of pre-existing helminth infection

Parasitol Res. 2018 Sep;117(9):2767-2784. doi: 10.1007/s00436-018-5965-9. Epub 2018 Jun 24.

Abstract

Although helminth-Plasmodium coinfections are common in tropical regions, the implications of this co-existence for the host immune response are poorly understood. In order to understand the effect of helminth infection at different times of coinfection on the immune response against Plasmodium infection, BALB/c mice were intraperitoneally infected with Taenia crassiceps (Tc). At 2 (Tc2) or 8 (Tc8) weeks post-infection, mice were intravenously infected with 1 × 103 Plasmodium yoelii (Py) 17XL-parasitized red blood cells. Py 17XL-single-infected mice developed cachexia, splenomegaly, and anemia, and died at 11 days post-infection. Importantly, Tc2 + Py-coinfected mice showed increased survival of 58% on day 11, but developed pathology (cachexia and splenomegaly) and succumbed on day 18 post-coinfection, this latter associated with high levels of IL-1β and IL-12, and reduced IFN-γ in serum compared with Py 17XL-single-infected mice. Interestingly, Tc8 + Py-coinfected mice showed increased survival up to 80% on day 11 and succumbed on day 30 post-coinfection. This increased survival rate conferred by chronic helminth infection was associated with a decreased pathology and mixed inflammatory-type 1/anti-inflammatory-type 2 immune profile as evidenced by the production of high levels of IL-12 and IL-10, and reduced TNF-α from macrophages, high levels of IL-4 and IL-10, and low levels of IFN-γ from spleen cells. Also high serum levels of IL-1β, TNF-α, IL-12, IL-4, and IL-10, but a significant reduction of IFN-γ were observed. Together, these data indicate that polarization of the cell-mediated response modulated by a pre-existing helminth infection differentially impacts on the host immune response to Py 17XL in a time-dependent manner.

Keywords: Co-infection; Helminths; Host-pathogen interaction; Malaria; Mixed infections; Plasmodium yoelii 17XL; Taenia crassiceps.

MeSH terms

  • Anemia
  • Animals
  • Cells, Cultured
  • Coinfection / parasitology*
  • Erythrocytes / parasitology
  • Female
  • Interleukin-10 / blood
  • Interleukin-12 Subunit p35 / blood
  • Macrophages / immunology
  • Malaria / blood
  • Malaria / immunology*
  • Malaria / pathology
  • Mice
  • Mice, Inbred BALB C
  • Plasmodium yoelii / immunology*
  • Spleen / immunology
  • Splenomegaly / parasitology
  • Taenia / immunology*
  • Taeniasis / blood
  • Taeniasis / immunology*
  • Taeniasis / pathology
  • Tumor Necrosis Factor-alpha / blood

Substances

  • IL10 protein, mouse
  • Il12a protein, mouse
  • Interleukin-12 Subunit p35
  • Tumor Necrosis Factor-alpha
  • Interleukin-10