TY - JOUR
T1 - Helminth infection is associated with dampened cytokine responses to viral and bacterial stimulations in Tsimane forager-horticulturalists
AU - Schneider-Crease, India A.
AU - Blackwell, Aaron D.
AU - Kraft, Thomas S.
AU - Emery Thompson, Melissa
AU - Maldonado Suarez, Ivan
AU - Cummings, Daniel K.
AU - Stieglitz, Jonathan
AU - Snyder-Mackler, Noah
AU - Gurven, Michael
AU - Kaplan, Hillard
AU - Trumble, Benjamin C.
N1 - Funding Information: This research was funded by the NIH/NIA (R01AG024119, RF1AG054442) and the ASU Center for Evolution and Medicine. J.S. acknowledges IAST funding from the French National Research Agency (ANR) ANR-17-EURE- 0010 (Investissements d'Avenir program). Publisher Copyright: © 2021 The Author(s).
PY - 2021
Y1 - 2021
N2 - 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-α). 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.
AB - 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-α). 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.
KW - bacteria
KW - cytokine storms
KW - eosinophilia
KW - hygiene hypothesis
KW - hypereosinophilia
KW - immunomodulation
KW - old friends hypothesis
KW - soil-transmitted helminths
KW - viruses
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U2 - 10.1093/emph/eoab035
DO - 10.1093/emph/eoab035
M3 - Article
SN - 2050-6201
VL - 9
SP - 349
EP - 359
JO - Evolution, Medicine and Public Health
JF - Evolution, Medicine and Public Health
IS - 1
ER -