Life history, immune function, and intestinal helminths: Trade‐offs among immunoglobulin E, C‐reactive protein, and growth in an Amazonian population

Abstract

Objectives Infection with helminths is associated with shifts in host immunity, including increased production of immunoglobulin E (IgE) and reduced inflammation. Given limited energy budgets, these shifts may involve changes in energy allocation toward competing demands. Here we test for potential trade-offs between growth, IgE, and the inflammatory marker C-reactive protein (CRP). Methods Dried blood spots and anthropometrics were collected from 162 Shuar forager-horticulturalists from a village in southeastern Ecuador. Enzyme-linked immunosorbent assays (ELISAs) were used to measure IgE and CRP. Relationships among IgE, CRP, and anthropometrics were examined in three groups: children aged 2–7 years (n = 63), children aged 8–15 (n = 61), and adults over age 18 (n = 37). Results Geometric mean IgE was 1,196 IU ml−1 while geometric mean CRP was 1.33 mg l−1. In children, IgE and CRP were negatively correlated (r = −0.21, P = 0.02, df = 122). Controlling for fat stores and age, IgE was associated with lower stature in children (t = −2.04, P = 0.04, df = 109), and adults (t = −3.29, P < 0.01, df = 33). In children there was a significant interaction between age and CRP, such that in younger children CRP was associated with shorter stature, but in older children was associated with greater stature (t = 2.15, P = 0.04, df = 109). Conclusions These results suggest that infection with helminths may have hidden costs associated with immunological changes, and that these costs may ultimately affect growth and other life history parameters.

Implications of market integration for cardiovascular and metabolic health among an indigenous Amazonian Ecuadorian population

“…Ages were determined by birthdates on government identification cards and the collection of extensive genealogical information, which included details about siblings and offspring, in order of birth. Overlapping genealogies were collected from multiple informants to cross-check information (Blackwell et al 2010). Pregnant women were not included in the study.…”

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“…It is also worth nothing that even in the absence of malnutrition and more virulent coinfecting species, coinfection in the Tsimane was associated with increased infection intensity. Previously, we have also shown that early and chronic elevated IgE-characteristic of endemic helminth exposure-is also associated with growth defi cits (Blackwell et al 2010 ). Thus, endemic exposure to multiple helminths may be a signifi cant cause of morbidity in the Tsimane.…”

“…These results have implications for vaccination programs and the spread of epidemic diseases among the Tsimane and require further investigation. Other work has suggested that early and chronic elevated IgE, characteristic of endemic helminth exposure, is also associated with growth defi cits (Blackwell et al 2010 ). Therefore, helminth infection may still pose a substantial threat to health and well-being in the Tsimane and other nonindustrialized populations.…”

“…In the absence of helminth and commensal-induced immunoregulation, infl ammation may be excessive, leading to autoimmune disorders such as arthritis. Previously we have shown that IgE, a marker of past and current helminth infection, is associated with lower infl ammatory markers, such as CRP (Blackwell et al 2010 ), and lower total cholesterol (Vasunilashorn et al 2010 ). However, as observed in the Tsimane, helminth infection may have varying effects on comorbidity during different life stages, with different clinical implications.…”

“…First, helminth-induced immunoregulation, which downregulates proinfl ammatory responses, may decrease resistance to other parasites and more virulent pathogens, resulting in increased infection intensity or exacerbated immunopathology (Graham et al 2005 ;Pullan and Brooker 2008 ). Second, exposure to helminth coinfection may increase investment in immune function (Bordes and Morand 2009 ), which may divert energy away from other fi tness-enhancing allocations, such as growth and reproduction (Sheldon and Verhulst 1996 ;Adamo 2001 ;Uller et al 2006 ;Blackwell et al 2010 ;Muehlenbein et al 2010 ). Given the risk of helminth coinfection in ancestral environments, potentially divergent immune responses, and the costs of increased investment in immune function, several questions arise.…”