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

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. 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 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. Infection with parasitic worms, known as helminths, alters the immune system, causing individuals to produce high levels of a type of antibody known as immunoglobulin E (IgE). IgE is typically very low in western populations, but is many times higher where helminth infections are common, particularly indigenous populations in South America. Helminths infect more than one seventh of the world's population. Since helminths tend to infect people at younger ages in areas where they are more common, a disproportionate number of those affected are schoolchildren. In this paper we examine IgE levels in two indigenous South American groups in comparison to levels in the United States. In these groups we find that IgE levels are not only higher, but that they also reach their highest levels at earlier ages in more infected populations. This finding is important since effects on immune function, including IgE production, may have additional consequences if they occur at young ages, changing the development of allergy and asthma, growth, and response to vaccines.