Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane forager-horticulturalists

India A Schneider-Crease; Aaron D Blackwell; Thomas S Kraft; Melissa Emery Thompson; Ivan Maldonado Suarez; Daniel K Cummings; Jonathan Stieglitz; Noah Snyder-Mackler; Michael Gurven; Hillard Kaplan; Benjamin C Trumble

doi:10.1093/emph/eoab035

Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane forager-horticulturalists

Evol Med Public Health. 2021 Oct 26;9(1):349-359. doi: 10.1093/emph/eoab035. eCollection 2021.

Authors

Affiliations

¹ Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA.
² Department of Anthropology, Washington State University, Pullman, WA, USA.
³ Department of Anthropology, University of California Santa Barbara, Santa Barbara, CA, USA.
⁴ Department of Anthropology, University of New Mexico, Albuquerque, NM, USA.
⁵ Tsimane Health and Life History Project, San Borja, Bolivia.
⁶ Economic Science Institute, Chapman University, Orange, CA, USA.
⁷ Institute for Advanced Study in Toulouse, Toulouse, France.
⁸ School of Life Sciences, Arizona State University, Tempe, AZ, USA.
⁹ School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA.

Abstract

Background: Soil-transmitted helminths (STHs) and humans share long co-evolutionary histories over which STHs have evolved strategies to permit their persistence by downregulating host immunity. Understanding the interactions between STHs and other pathogens can inform our understanding of human evolution and contemporary disease patterns.

Methodology: We worked with Tsimane forager-horticulturalists in the Bolivian Amazon, where STHs are prevalent. We tested whether STHs and eosinophil levels-likely indicative of infection in this population-are associated with dampened immune responses to in vitro stimulation with H1N1 and lipopolysaccharide (LPS) antigens. Whole blood samples (n = 179) were treated with H1N1 vaccine and LPS and assayed for 13 cytokines (INF-γ, IL-1β, IL-2, IL-4, IL-5, IL-6, IL-7, IL-8, IL-10, IL-12p70, IL-13, GM-CSF and TNF-ɑ). We evaluated how STHs and eosinophil levels affected cytokine responses and T helper (Th) 1 and Th2-cytokine suite responses to stimulation.

Results: Infection with Ascaris lumbricoides was significantly (P ≤ 0.05) associated with lower response of some cytokines to H1N1 and LPS in women. Eosinophils were significantly negatively associated with some cytokine responses to H1N1 and LPS, with the strongest effects in women, and associated with a reduced Th1- and Th2-cytokine response to H1N1 and LPS in women and men.

Conclusions and implications: Consistent with the 'old friends' and hygiene hypotheses, we find that STHs were associated with dampened cytokine responses to certain viral and bacterial antigens. This suggests that STH infections may play an essential role in immune response regulation and that the lack of STH immune priming in industrialized populations may increase the risk of over-reactive immunity. Lay Summary: Indicators of helminth infection were associated with dampened cytokine immune responses to in vitro stimulation with viral and bacterial antigens in Tsimane forager-horticulturalists in the Bolivian Amazon, consistent with the 'old friends' and hygiene hypotheses.

Keywords: bacteria; cytokine storms; eosinophilia; hygiene hypothesis; hypereosinophilia; immunomodulation; old friends hypothesis; soil-transmitted helminths; viruses.

Abstract

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