Zoonotic helminth exposure and risk of allergic diseases: A study of two generations in Norway

Clin Exp Allergy. 2018;48:66–77.

N. O. Jogi1,2, C. Svanes2,3, S. P. Siiak1, E. Logan4, J. W. Holloway5J. Igland6, A. Johannessen2, M. Levin4, F. G. Real7, V. Schlunssen8,9W. G. C. Horsnell10,11,12, R. J. Bertelsen3,7

 

1 University of Tartu, Tartu, Estonia

2 Centre for International Health, University of Bergen, Bergen, Norway

3 Department of Occupational Medicine, Haukeland University Hospital, Bergen, Norway

4 University of Cape Town, Cape Town, South Africa

5 Human Development & Health, Faculty of Medicine, University of Southampton, Southampton, UK

6 Department of Global Public Health and Primary Care, University of Bergen, Bergen, Norway

7 Department of Clinical Science, University of Bergen, Bergen, Norway

8 Aarhus University, Aarhus, Denmark

9 National Research Centre for the Working Environment, Copenhagen, Denmark

10 Institute of Infectious Disease and Molecular Medicine/Division of Immunology, University of Cape Town, Cape Town, South Africa

11 Institute of Microbiology and Infection, University of Birmingham, Birmingham, UK

12 Laboratory of Molecular and Experimental Immunology and Neurogenetics, UMR 7355, CNRS-University of Orleans and Le Studium Institute for Advanced Studies, Orleans, France

Correspondence R. J. Bertelsen, Department of Clinical Science, University of Bergen, Bergen, Norway. Email: randi.j.bertelsen@uib.no

Abstract

Background: Animal and human studies indicate that definitive host helminth infections may confer protection from allergies. However, zoonotic helminths, such as Toxocara species (spp.), have been associated with increased allergies. Objective: We describe the prevalence of Toxocara spp. and Ascaris spp. seropositivity and associations with allergic diseases and sensitization, in 2 generations in Bergen, Norway. Methods: Serum levels of total IgG4, anti-Toxocara spp. IgG4 and Ascaris spp. IgG4 were established by ELISA in 2 cohorts: parents born 1945-1972 (n = 171) and their offspring born 1969-2003 (n = 264). Allergic outcomes and covariates were recorded through interviews and clinical examinations including serum IgEs and skin prick tests. Results: Anti-Ascaris spp. IgG4 was detected in 29.2% of parents and 10.3% of offspring, and anti-Toxocara spp. IgG4 in 17.5% and 8.0% of parents and offspring, respectively. Among offspring, anti-Toxocara spp. IgG4 was associated with pet keeping before age 15 (OR = 6.15; 95% CI = 1.37-27.5) and increasing BMI (1.16 [1.06-1.25] per kg/m2). Toxocara spp. seropositivity was associated with wheeze (2.97[1.45- 7.76]), hayfever (4.03[1.63-9.95]), eczema (2.89[1.08-7.76]) and cat sensitization (5.65[1.92-16.6]) among offspring, but was not associated with allergic outcomes among parents. Adjustment for childhood or current pet keeping did not alter associations with allergies. Parental Toxocara spp. seropositivity was associated with increased offspring allergies following a sex-specific pattern. Conclusions & Clinical Relevance: Zoonotic helminth exposure in Norway was less frequent in offspring than parents; however, Toxocara spp. seropositivity was associated with increased risk of allergic manifestations in the offspring generation, but not among parents. Changes in response to helminth exposure may provide insights into the increase in allergy incidence in affluent countries.

Keywords

Allergy
Ascaris
Asthma
ECRHS
Helminths
IgG4
Norway
RHINESSA
Toxocara
Zoonosis
Published by

Wiley