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

Author:

Schneider-Crease India A1ORCID,Blackwell Aaron D2ORCID,Kraft Thomas S3,Emery Thompson Melissa4,Maldonado Suarez Ivan5,Cummings Daniel K6,Stieglitz Jonathan7ORCID,Snyder-Mackler Noah18,Gurven Michael3ORCID,Kaplan Hillard6,Trumble Benjamin C189

Affiliation:

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

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.

Funder

NIH/NIA

Publisher

Oxford University Press (OUP)

Subject

Health, Toxicology and Mutagenesis,Ecology, Evolution, Behavior and Systematics,Medicine (miscellaneous)

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