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.

<h4>Background</h4>The 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 increas...

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Main Authors: Aaron D Blackwell, Michael D Gurven, Lawrence S Sugiyama, Felicia C Madimenos, Melissa A Liebert, Melanie A Martin, Hillard S Kaplan, J Josh Snodgrass
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-06-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0001218&type=printable
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author Aaron D Blackwell
Michael D Gurven
Lawrence S Sugiyama
Felicia C Madimenos
Melissa A Liebert
Melanie A Martin
Hillard S Kaplan
J Josh Snodgrass
author_facet Aaron D Blackwell
Michael D Gurven
Lawrence S Sugiyama
Felicia C Madimenos
Melissa A Liebert
Melanie A Martin
Hillard S Kaplan
J Josh Snodgrass
author_sort Aaron D Blackwell
collection DOAJ
description <h4>Background</h4>The 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.<h4>Methodology/principal findings</h4>Total 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.<h4>Conclusions</h4>The 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.
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spelling doaj.art-446371c81fcc4e459856c959cf59f91a2025-02-20T05:31:51ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352011-06-0156e121810.1371/journal.pntd.0001218Evidence 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.Aaron D BlackwellMichael D GurvenLawrence S SugiyamaFelicia C MadimenosMelissa A LiebertMelanie A MartinHillard S KaplanJ Josh Snodgrass<h4>Background</h4>The 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.<h4>Methodology/principal findings</h4>Total 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.<h4>Conclusions</h4>The 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.https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0001218&type=printable
spellingShingle Aaron D Blackwell
Michael D Gurven
Lawrence S Sugiyama
Felicia C Madimenos
Melissa A Liebert
Melanie A Martin
Hillard S Kaplan
J Josh Snodgrass
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.
PLoS Neglected Tropical Diseases
title 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.
title_full 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.
title_fullStr 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.
title_full_unstemmed 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.
title_short 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.
title_sort 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
url https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0001218&type=printable
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