Evidence for a Peak Shift in a Humoral Response to Helminths: Age Profiles of IgE in the Shuar of Ecuador, the Tsimane of Bolivia, and the U.S. NHANES

Abstract

BackgroundThe peak shift model predicts that the age-profile of a pathogen's prevalence depends upon its transmission rate, peaking earlier in populations with higher transmission and declining as partial immunity is acquired. Helminth infections are associated with increased immunoglobulin E (IgE), which may convey partial immunity and influence the peak shift. Although studies have noted peak shifts in helminths, corresponding peak shifts in total IgE have not been investigated, nor has the age-patterning been carefully examined across populations. We test for differences in the age-patterning of IgE between two South American forager-horticulturalist populations and the United States: the Tsimane of Bolivia (n = 832), the Shuar of Ecuador (n = 289), and the U.S. NHANES (n = 8,336). We then examine the relationship between total IgE and helminth prevalences in the Tsimane.Methodology/Principal FindingsTotal IgE levels were assessed in serum and dried blood spots and age-patterns examined with non-linear regression models. Tsimane had the highest IgE (geometric mean = 8,182 IU/ml), followed by Shuar (1,252 IU/ml), and NHANES (52 IU/ml). Consistent with predictions, higher population IgE was associated with steeper increases at early ages and earlier peaks: Tsimane IgE peaked at 7 years, Shuar at 10 years, and NHANES at 17 years. For Tsimane, the age-pattern was compared with fecal helminth prevalences. Overall, 57% had detectable eggs or larva, with hookworm (45.4%) and Ascaris lumbricoides (19.9%) the most prevalent. The peak in total IgE occurred around the peak in A. lumbricoides, which was associated with higher IgE in children <10, but with lower IgE in adolescents.ConclusionsThe age-patterning suggests a peak shift in total IgE similar to that seen in helminth infections, particularly A. lumbricoides. This age-patterning may have implications for understanding the effects of helminths on other health outcomes, such as allergy, growth, and response to childhood vaccination.

Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics

“…THLHP researchers work extensively in Tsimane villages, collecting demographic, anthropological and biomedical data, while also providing primary medical care. Helminth infections are highly prevalent, infecting 57% of the population [19].…”

“…Following on-site analysis of participant blood and faecal samples, physicians administered vitamins, antibiotics, anti-protozans and anti-helminthics as warranted. Ethnographic and epidemiological information on the Tsimane, methods for age estimation, subject sampling, biomarker collection and physician diagnostics have been described elsewhere [19,20].…”

“…Beginning in 2007, faecal samples were also preserved in 10% formalin solution following direct identification, and later analysed using a modified Percoll (Amersham Pharmacia) technique [23]. As we report elsewhere, the Percoll method identified slightly more positive cases, but did not produce systematic biases in parasite identification [19]. We therefore coded individuals as positive or negative for identified species in a single dataset, regardless of which method was used.…”

Allergic disorders and socio‐economic status: a study of schoolchildren in an urban area of Makassar, Indonesia

“…In the high-SES school where the prevalence of T. trichiura was much lower, infection with this parasite was not significantly associated with the increased levels of total IgE, suggesting that levels of total IgE in low-SES school are likely to be the consequence of higher transmission of T. trichiura and other helminth such as A. lumbricoides which was also prevalent in low-SES school. In line with this, a study by Blackwell et al [37] showed that in rural Ecuador and Bolivia, total IgE increased with increasing helminth positivity and decreased in parallel with reduction of helminth infestation [38].…”

Lethality of First Contact Dysentery Epidemics on Pacific Islands

“…47 Additional risk factors could have been due to the very narrow genomic base of such isolated populations which would have produced a high level of human leukocyte antigen homogeneity through a founder effect or a Th2 bias created by exposure to a very limited set of pathogens such as helminths. [48][49][50] In dysentery, disruption of the stable enteric ecosystem by a single pathogen was magnified by the host response into a dysfunctional inflammatory reaction that presented as dysentery. Death was through a protein-losing enteropathy that further degraded the host's ability to respond to infections not unlike those seen in severely malnourished groups such as prisoners of war.…”