Soil‐transmitted helminth infection and intestinal inflammation among the Shuar of Amazonian Ecuador

Abstract

Objectives: Little research exists documenting levels of intestinal inflammationamong indigenous populations where exposure to macroparasites, like soil-transmitted helminths (STHs), is common. Reduced STH exposure is hypothesized to contribute to increased prevalence of elevated intestinal inflammation in wealthy nations, likely due to coevolutionary histories between STHs and human immune systems that favored anti-inflammatory pathways. Here, we document levels of intestinal inflammation and test associations with STH infection among the Shuar of Ecuador, an indigenous population undergoing socioeconomic/lifestyle changes that influence their hygienic environment. We predict that fecal calprotectin (FC; a measure of intestinal inflammation) will be lower in STH infected individuals and that FC will be negatively associated with infection intensity.Methods: Stool samples to analyze FC levels and STH infection were collected from 69 Shuar participants (ages 5-75 years). Children (<15 years) and adults (15+ years) were analyzed separately to understand the role of exposure in immune system development and the intestinal inflammatory response.Results: Two species of STH were present: Ascaris lumbricoides and Trichuris trichiura.The relationships between infection and intestinal inflammation were age-and species-specific. While no significant relationships were found among adults, children who were singly infected with T. trichiura had lower FC levels than uninfected children. Infection intensity was not significantly associated with FC in children or adults.Conclusions: These preliminary results provide limited support for our hypotheses, documenting tentative age-and species-specific associations between FC and infection status. Findings may point to the importance of species-specific STH exposure during immune system development. K E Y W O R D Sfecal calprotectin, hygiene hypothesis, inflammatory bowel disease, old friends hypothesis, soil-transmitted helminths

Measuring attack on self: The need for field‐friendly methods development and research on autoimmunity in human biology

“…These findings among the Shuar are noteworthy because Shuar generally have low levels of inflammatory biomarkers and no evidence of chronic inflammation compared to WEIRD populations (Cepon‐Robins et al, 2019; McDade et al, 2012), suggesting that environmental factors, like pathogen exposure, are regulating immune function. This, however, cannot be accounted for by pathogen exposure alone, since other indigenous populations like the Tsimane have both high parasite loads and high CRP (Blackwell et al, 2016), indicating that more population‐based research needs to be conducted to fully understand these relationships.…”

“…Previous research in human biology has shown that parasite exposure may reduce both systemic and local inflammation (Cepon‐Robins et al, 2019; Robins, 2015). Work among the Shuar of Amazonian Ecuador showed that adults who were infected with Ascaris lumbricoides (i.e., intestinal parasitic large roundworm) had significantly lower CRP levels (Robins, 2015).…”

“…Soil‐transmitted helminth infection status and intensity (Cepon, 2015; Cepon‐Robins et al, 2014, 2019; Gildner et al, 2016; Tanner et al, 2009)…”

“…Ultimately, this means that what we do know about autoimmunity comes from what have been termed “western, educated, industrialized, rich democracies” or “WEIRD” countries (Gurven & Lieberman, 2020). Indigenous, remote, and marginalized (i.e., non‐WEIRD) populations are hypothesized to have lower prevalence of AIID due to a greater exposure to infectious diseases and lifestyles that do not support a pro‐inflammatory phenotype (i.e., less‐processed food consumption, high physical activity levels, low rates of obesity) that regulate immune function (Bach, 2018; Cepon‐Robins et al, 2019; McDade et al, 2012; Rook, 2012), but, while theoretically sound this hypothesis is under‐tested (Figure 1). Even if true, a lack of AIID research among more remote, subsistence‐based populations may become problematic as these populations transition to more market‐integrated lifeways.…”

S100A8/S100A9 deficiency increases neutrophil activation and protective immune responses against invading infective L3 larvae of the filarial nematode Litomosoides sigmodontis

“…S100A8/A9 has been previously investigated as marker for intestinal inflammation with controversial results so far [67,68]. A negative association between children infected with the intestinal helminth Trichuris trichiura and decreased intestinal inflammation as well as decreased concentration of S100A8/A9 compared to uninfected children has been reported [69]. In contrast, there was no evidence of an association between S100A8/A9 levels and Schistosoma mansoni [70] or Ascaris lumbricoides infection [71].…”