Evidence of microbial translocation associated with perturbations in T cell and antigen-presenting cell homeostasis in hookworm infections

PLoS Negl Trop Dis. 2012;6(10):e1830. doi: 10.1371/journal.pntd.0001830. Epub 2012 Oct 4.

Abstract

Background: Microbial translocation (MT) is the process by which microbes or microbial products translocate from the intestine to the systemic circulation. MT is a common cause of systemic immune activation in HIV infection and is associated with reduced frequencies of CD4(+) T cells; no data exist, however, on the role of MT in intestinal helminth infections.

Methods: We measured the plasma levels of MT markers, acute-phase proteins, and pro- and anti-inflammatory cytokines in individuals with or without hookworm infections. We also estimated the absolute counts of CD4(+) and CD8(+) T cells as well as the frequencies of memory T cell and dendritic cell subsets. Finally, we also measured the levels of all of these parameters in a subset of individuals following treatment of hookworm infection.

Results: Our data suggest that hookworm infection is characterized by increased levels of markers associated with MT but not acute-phase proteins nor pro-inflammatory cytokines. Hookworm infections were also associated with increased levels of the anti-inflammatory cytokine--IL-10, which was positively correlated with levels of lipopolysaccharide (LPS). In addition, MT was associated with decreased numbers of CD8(+) T cells and diminished frequencies of particular dendritic cell subsets. Antihelmintic treatment of hookworm infection resulted in reversal of some of the hematologic and microbiologic alterations.

Conclusions: Our data provide compelling evidence for MT in a human intestinal helminth infection and its association with perturbations in the T cell and antigen-presenting cell compartments of the immune system. Our data also reveal that at least one dominant counter-regulatory mechanism i.e. increased IL-10 production might potentially protect against systemic immune activation in hookworm infections.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Antigen-Presenting Cells / immunology*
  • Bacterial Translocation*
  • Hookworm Infections / complications
  • Hookworm Infections / immunology*
  • Hookworm Infections / pathology*
  • Humans
  • Lymphocyte Count
  • Prospective Studies
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocytes / immunology*