Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment

doi:10.1016/S0091-6749(98)70386-0

Journal of Allergy and Clinical Immunology

Volume 101, Issue 2, February 1998, Pages 217-221

https://doi.org/10.1016/S0091-6749(98)70386-0 Get rights and content

Abstract

Background: Although IgE antibody is clearly involved in allergic reactions to environmental allergens, this immunoglobulin is an important component of host-protective immune responses against the helminthic parasites that are endemic in the majority of the world population. However, these infections not only stimulate the production of antiparasite IgE antibody but can nonspecifically induce polyclonal IgE synthesis that results in highly elevated total serum IgE levels. Such polyclonal stimulation can diminish specific IgE antibody responses and cause saturation of mast cell Fcϵ receptors, thus inhibiting allergic reactivity. This may represent a mechanism of immune evasion by the parasite.

Objective: Because an atopic disposition is generally recognized to be associated with elevated IgE synthesis against environmental allergens, the aim of this study was to evaluate the influence of atopy on the antiparasite response. To this end, we examined two groups of Venezuelan children in whom the intestinal helminth Ascaris lumbricoides is endemic but that differ greatly in their level of atopy. One group was from an island population (Coche Island) that has a very strong atopic background and in which the prevalence of allergic disease is extremely high. The other was a group of nonatopic children belonging to a mainland population (Barrio Los Erasos) that is of comparable socioeconomic level and has an exposure to helminthic infection similar to that of the island group but a relatively low expression of allergic diseases.

Results: Although the living conditions and the prevalence of Ascaris infection of the two groups were comparable, the intensity of the parasitic infection was considerably higher in the nonatopic mainland children (geometric mean values of eggs per gram of feces: Barrio Los Erasos, 7621; Coche Island, 1435; p < 0.001). In addition, their total serum IgE levels were significantly more elevated than in the atopic island group (geometric mean: Barrio Los Erasos, 2172; Coche Island, 941 IU/ml; p < 0.001). In contrast, the specific anti-Ascaris response was much stronger in the atopic children (geometric mean: Barrio Los Erasos, 0.30; Coche Island, 0.91 PRU/ml; p < 0.001), which resulted in the ratio of specific to total IgE being nine times higher than in the nonatopic mainland subjects. These differences were maintained even when the children were matched on the basis of infection intensity, thus indicating that the atopic children have an intrinsic propensity to favor specific over polyclonal IgE responses to the parasite.

Conclusions: The children with a strong atopic background demonstrated IgE responses concordant with an enhanced protective response against helminthic parasites and had significantly lower intensities of infection than their nonatopic counterparts. These observations support the concept that the atopic state has conferred a selective evolutionary advantage that could compensate for its involvement in allergic disease. (J Allergy Clin Immunol 1998;101:217-21.)

Section snippets

Study populations

Coche Island has a total population of approximately 7000 people, and the study group was selected at random with the use of census information from the four consolidated villages on the island. Informed parental consent to participate in the study was obtained for 626 children (56% female) between the ages of 2 and 12 years (mean ± standard deviation: 6.8 ± 2.9 years).

All of the approximately 300 family groups established in Barrio Los Erasos, a clearly delimited slum area of Caracas, were

Allergic disease in Coche Island children

Of the 626 children randomly selected from the island population, 380 (61%) were found to have a recent clinical history of asthma and/or rhinitis. Asthma was the predominant pathologic condition, with 92% of the symptomatic subjects reporting this compared with 35% with rhinitis. Although the establishment of a history of dermatologic allergy by questioning was somewhat difficult in this population, and conditions such as atopic dermatitis, urticaria, and angioedema were reported less

DISCUSSION

We have previously reported that the prevalence of allergic diseases, particularly asthma and rhinitis, in Venezuelan children from urban slum areas, such as the Barrio Los Erasos, is substantially lower than in children of higher socioeconomic levels, in which the prevalence is comparable to other areas of the world.11, 12, 13, 24 Evidence has been obtained to suggest that this is due at least in part to suppressive effects of the helminthic parasites that are endemic in such underprivileged

Acknowledgements

We thank Mr. D. Gonzalez and Mrs. Y. Barrios (MSAS, Maracay, Venezuela) for performing the Kato tests.

References (41)

HR Miller
Mucosal mast cells and the allergic response against nematode parasites
Vet Immunol Immunopathol
(1996)
F Finkelman et al.
Regulation and biological function of helminth-induced cytokine responses
Immunol Today
(1991)
I Hagel et al.
Relationship between the degree of poverty and the IgE response to Ascaris infection in slum children
Trans R Soc Trop Med Hyg
(1993)
NR Lynch et al.
Effect of antihelmintic treatment on the allergic reactivity of children in a tropical slum
J Allergy Clin Immunol
(1993)
NR Lynch et al.
Incidence of atopic disease in a tropical environment: partial independence from intestinal helminthiasis
J Allergy Clin Immunol
(1984)
KJ Turner et al.
Studies on bronchial hyperreactivity, allergic responsiveness, and asthma in rural and urban children of the highlands of Papua New Guinea
J Allergy Clin Immunol
(1986)
EE Jarrett et al.
Production and activities of IgE in helminth infection.
NR Lynch
Immediate hypersensitivity (allergic) reactions to intestinal helminthic infections
Baillieres Clin Trop Med Commun Dis
(1987)
R Moqbel et al.
Parasites and allergy: evidence for a 'cause and effect' relationship
Clin Exp Allergy
(1990)
RG Bell
IgE, allergies and helminth parasites: a new perspective on an old conundrum
Immunol Cell Biol
(1996)

M Capron et al.

Immunoglobulin E and effector cells in schistosomiasis

Science

(1994)

JE Allen et al.

Immunology of human helminth infection

Int Arch Allergy Immunol

(1996)

AE Butterworth et al.

Immunity and morbidity in Schistosoma mansoni infection: quantitative aspects

Am J Trop Med Hyg

(1996)

P Hagan

Immunity and morbidity in infection due to Schistosoma haematobium

Am J Trop Med Hyg

(1996)

BJ Sutton et al.

The human IgE network

Nature

(1993)

NR Lynch et al.

High allergic reactivity in a tropical environment

Clin Allergy

(1984)

NR Lynch et al.

Allergic reactivity and socio-economic level in a tropical environment

Clin Allergy

(1987)

I Hagel et al.

Allergic reactivity of children of different socioeconomic levels in tropical populations

Int Arch Allergy Immunol

(1993)

PG Holt

Environmental factors and primary T-cell sensitisation to inhalant allergens in infancy: reappraisal of the role of infections and air pollution

Pediatr Allergy Immunol

(1995)

WO Cookson et al.

Asthma: an epidemic in the absence of infection?

Science

(1997)

Cited by (168)

Poorly controlled asthma – Easy wins and future prospects for addressing fungal allergy
2023, Allergology International
Poorly controlled asthma is especially common in low resource countries. Aside from lack of access to, or poor technique with, inhaled beta-2 agonists and corticosteroids, the most problematic forms of asthma are frequently associated with both fungal allergy and exposure, especially in adults leading to more asthma exacerbations and worse asthma. The umbrella term ‘fungal asthma’ describes many disorders linked to fungal exposure and/or allergy to fungi. One fungal asthma endotype, ABPA, is usually marked by a very high IgE and its differential diagnosis is reviewed. Both ABPA and fungal bronchitis in bronchiectasis are marked by thick excess airway mucus production. Dermatophyte skin infection can worsen asthma and eradication of the skin infection improves asthma. Exposure to fungi in the workplace, home and schools, often in damp or water-damaged buildings worsens asthma, and remediation improves symptom control and reduces exacerbations. Antifungal therapy is beneficial for fungal asthma as demonstrated in nine of 13 randomised controlled studies, reducing symptoms, corticosteroid need and exacerbations while improving lung function. Other useful therapies include azithromycin and some biologics approved for the treatment of severe asthma. If all individuals with poorly controlled and severe asthma could be ‘relieved’ of their fungal allergy and infection through antifungal therapy without systemic corticosteroids, the health benefits would be enormous and relatively inexpensive, improving the long term health of over 20 million adults and many children. Antifungal therapy carries some toxicity, drug interactions and triazole resistance risks, and data are incomplete. Here we summarise what is known and what remains uncertain about this complex topic.
Endocannabinoid modulation of allergic responses: Focus on the control of FcεRI-mediated mast cell activation
2023, European Journal of Cell Biology
Allergic reactions are highly prevalent pathologies initiated by the production of IgE antibodies against harmless antigens (allergens) and the activation of the high-affinity IgE receptor (FcεRI) expressed in the surface of basophils and mast cells (MCs). Research on the mechanisms of negative control of those exacerbated inflammatory reactions has been intense in recent years. Endocannabinoids (eCBs) show important regulatory effects on MC-mediated immune responses, mainly inhibiting the production of pro-inflammatory mediators. However, the description of the molecular mechanisms involved in eCB control of MC activation is far from complete. In this review, we aim to summarize the available information regarding the role of eCBs in the modulation of FcεRI-dependent activation of that cell type, emphasizing the description of the eCB system and the existence of some of its elements in MCs. Unique characteristics of the eCB system and cannabinoid receptors (CBRs) localization and signaling in MCs are mentioned. The described and putative points of cross-talk between CBRs and FcεRI signaling cascades are also presented. Finally, we discuss some important considerations in the study of the effects of eCBs in MCs and the perspectives in the field.
Cellular immune response of asthmatic children in the presence of anti-Ascaris antibody
2020, Immunobiology
The presence of anti-Ascaris (anti-Asc) immunoglobin isotypes alters the risk of allergic asthma. In this study, we analyzed the relationships between serum levels of anti-Asc IgE, IgG1, and IgG4, without concurrent infection by the parasite, and the presence of asthma. We measured cytokine levels from Th1, Th2, and Th17 profiles. Children aged 2–14 years old, asthmatics (n = 64), and non-asthmatics (n = 40) were selected according to the International Study of Asthma and Allergies in Childhood criteria. Asthmatic patients who had positive skin allergy tests were considered to have allergic asthma. Stool exams were performed to exclude children who were parasitized by helminths/protozoans and blood samples were collected in non-parasitized individuals. We performed peripheral blood leukocyte counts and in vitro culture following mitogenic stimulation. Levels of cytokines (IL-2, IL-4, IL-6, IL-10, TNF-α, IFN-γ, and IL-17) in the supernatants were measured using a cytometric bead array. Titration of serum total IgE and IgE specific to Ascaris were obtained using ImmunoCAP; IgG1 and IgG4 titers were measured using enzyme-linked immunosorbent assays. Anti-Asc IgE was associated with a higher risk of asthma and an increase in the number of eosinophils and neutrophils. By contrast, anti-Asc IgG1 could be considered a protective factor against asthma, associated with lower levels of circulating neutrophils. There were high levels of IL-6 and TNF-α in asthmatics. Levels of IL-6, but not TNF-α, depended on the presence of anti-Asc IgG1 in serum. Anti-Asc IgE appears to increase risk of asthma, and anti-Asc IgG1 appears to favor decreased neutrophil counts and increased IL-6 levels.
Characterization of subtypes of Blastocystis sp. isolated from patients with urticaria, São Paulo, Brazil
2019, Parasite Epidemiology and Control
Blastocystis sp. is described as an enteric protist prevalent in fecal samples from humans and animals; its pathogenicity and epidemiology are still controversial. Currently, it has been associated with intestinal diseases such as irritable bowel syndrome and clinical manifestations of allergic skin, such as chronic urticaria. In the context of urticaria, it is still uncertain whether this organism is directly related to the allergic manifestation or just a common component of the intestinal microbiota. This study aimed to evaluate the occurrence and molecular diversity of Blastocystis sp. in individuals with urticaria from a dermatology outpatient clinic, São Paulo, Brazil. Fecal samples of 58 patients with urticaria were examined using parasitological methods; and subsequently tested by polymerase chain reaction using Blastocystis-specific primers. The subtypes (STs) and alleles (a) were determined using BLASTn and MLST tools. ST1, ST2, ST3, ST4, ST6 and mixed infection (ST1 + ST3) were identified in the patients with urticaria; ST1 (a4), ST3 (a34 and a36) and ST4 (a42) were the most prevalent. Our molecular analyses allowed an initial description of Blastocystis subtypes in patients with urticaria from São Paulo city, Brazil.
Biologics for Asthma and Risk of Infection: Cause for Concern?
2019, Immunology and Allergy Clinics of North America
Serodiagnosis and early detection of Strongyloides stercoralis infection
2019, Journal of Microbiology, Immunology and Infection
Strongyloidiasis is a major neglected tropical disease with the potential of causing lifelong infection and mortality. One of the ways for effective control of this disease is developing improved diagnostics, particularly using serological approaches. A serological test can achieve high diagnostic sensitivity and specificity, has the potential for point-of-care translation, and can be used as a screening tool for early detection. More research is needed to find clinically important antibody biomarkers for early disease detection, mapping, and epidemiological surveillance. This article summarizes human strongyloidiasis and the available diagnostic tools for the disease, focusing on describing the current antibody assays for strongyloidiasis. Finally, prospects of developing a more effective serodiagnostic tool for strongyloidiasis are discussed.

View all citing articles on Scopus

^☆: From ^aInstituto de Biomedicina, Universidad Central de Venezuela, Caracas; ^bClinica Experimental de Asma, FONDENE, Edo., Nueva Esparta; ^cHospital Miguel Perez-Carreño, Caracas; ^dHospital de Niños J.M. de los Rios, Caracas; ^eInstituto de Medicinal Tropical, Universidad Central de Venezuela, Caracas; and ^fDepartment of Paediatrics, Faculty of Medicine, University of Western Australia, Perth.

^☆☆: Supported by CONICIT project RPV 170041, CDCH/UCV, World Bank VEN/96/002/14 (Venezuela), NH and MRC (Australia), and grant SD-000-0309 from Astra-Draco (Sweden).

^★: Reprint requests: Neil Lynch, PhD, Instituto de Biomedicina, Aptdo. 4043, Caracas 1010, Venezuela.

^★★: 1/1/86219

View full text

Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment☆,☆☆,★,★★

Abstract

Section snippets

Study populations

Allergic disease in Coche Island children

DISCUSSION

Acknowledgements

Vet Immunol Immunopathol

Immunol Today

Trans R Soc Trop Med Hyg

J Allergy Clin Immunol

J Allergy Clin Immunol

J Allergy Clin Immunol

Production and activities of IgE in helminth infection.

Immediate hypersensitivity (allergic) reactions to intestinal helminthic infections

Baillieres Clin Trop Med Commun Dis

Parasites and allergy: evidence for a 'cause and effect' relationship

Clin Exp Allergy

IgE, allergies and helminth parasites: a new perspective on an old conundrum

Immunol Cell Biol

Immunoglobulin E and effector cells in schistosomiasis

Science

Immunology of human helminth infection

Int Arch Allergy Immunol

Immunity and morbidity in Schistosoma mansoni infection: quantitative aspects

Am J Trop Med Hyg

Immunity and morbidity in infection due to Schistosoma haematobium

Am J Trop Med Hyg

The human IgE network

Nature

High allergic reactivity in a tropical environment

Clin Allergy

Allergic reactivity and socio-economic level in a tropical environment

Clin Allergy

Allergic reactivity of children of different socioeconomic levels in tropical populations

Int Arch Allergy Immunol

Environmental factors and primary T-cell sensitisation to inhalant allergens in infancy: reappraisal of the role of infections and air pollution

Pediatr Allergy Immunol

Asthma: an epidemic in the absence of infection?

Science