Helminths are positively associated with atopy and wheeze in Ugandan fishing communities: results from a cross‐sectional survey

Abstract

BackgroundParasitic helminths are potent immunomodulators and chronic infections may protect against allergy‐related disease and atopy. We conducted a cross‐sectional survey to test the hypothesis that in heavily helminth‐exposed fishing villages on Lake Victoria, Uganda, helminth infections would be inversely associated with allergy‐related conditions.MethodsA household survey was conducted as baseline to an anthelminthic intervention trial. Outcomes were reported wheeze in last year, atopy assessed both by skin prick test (SPT) and by the measurement of allergen‐specific IgE to dust mites and cockroach in plasma. Helminth infections were ascertained by stool, urine and haemoparasitology. Associations were examined using multivariable regression.ResultsTwo thousand three hundred and sixteen individuals were surveyed. Prevalence of reported wheeze was 2% in under‐fives and 5% in participants ≥5 years; 19% had a positive SPT; median Dermatophagoides‐specific IgE and cockroach‐specific IgE were 1440 and 220 ng/ml, respectively. S. mansoni, N. americanus, S. stercoralis, T. trichiura, M. perstans and A. lumbricoides prevalence was estimated as 51%, 22%, 12%, 10%, 2% and 1%, respectively. S. mansoni was positively associated with Dermatophagoides‐specific IgE [adjusted geometric mean ratio (aGMR) (95% confidence interval) 1.64 (1.23, 2.18)]; T. trichiura with SPT [adjusted odds ratio (aOR) 2.08 (1.38, 3.15)]; M. perstans with cockroach‐specific IgE [aGMR 2.37 (1.39, 4.06)], A. lumbricoides with wheeze in participants ≥5 years [aOR 6.36 (1.10, 36.63)] and with Dermatophagoides‐specific IgE [aGMR 2.34 (1.11, 4.95)]. No inverse associations were observed.ConclusionsContrary to our hypothesis, we found little evidence of an inverse relationship between helminths and allergy‐related outcomes, but strong evidence that individuals with certain helminths were more prone to atopy in this setting.

Parasites and allergy: Observations from Africa

“…Although this is not a meta‐analysis, the total numbers of participants in the various studies are shown. Two of the three studies that showed a positive association were of Ascaris and respiratory symptoms of wheeze or exercise‐induced bronchospasms, and the third between Trichuris and SPT . Although migration of Ascaris larva through the lungs is mostly asymptomatic, on rare occasions this may be associated with respiratory symptoms such as wheezing, dyspnoea and bronchospasm .…”

“…Of the six studies that showed an inverse association between helminths and allergy‐related outcomes (in Table ), five of them were conducted in areas with a high proportion of individuals infected with helminths, while the sixth study was conducted in an area with low proportion of individuals infected with helminths . It is also important to note that although a study conducted among island communities in Lake Victoria where the proportion of individuals with helminth infections was high, no inverse associations with allergy‐related outcomes were reported …”

Worms: Pernicious parasites or allies against allergies?

“…However, in helminth‐endemic areas (especially rural areas of low socioeconomic status), this relationship often breaks down . Furthermore, multiple epidemiological studies have shown a positive association between antihelminth IgE (ascariasis, schistosomiasis, filariasis) and wheeze and/or atopy . One of the reasons for discrepancies between IgE reactivity (against allergen or helminth) and allergy in high‐income versus helminth‐endemic areas might be due to cross‐reactivity of antihelminth IgE to certain allergens.…”

Parasites and allergy: Observations from Brazil

“…Epidemiological evidence from the published literature for an effect of helminths on allergy is contradictory; while some studies have indicated a positive association with allergy, others have not . The actual effects of helminths and allergies in a particular population may be affected by a number of factors including the age of first infection, duration and chronicity of infections, parasite burden, the parasite species present and the host genetic background of that population .…”