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

N O Jõgi; C Svanes; S P Siiak; E Logan; J W Holloway; J Igland; A Johannessen; M Levin; F G Real; V Schlunssen; W G C Horsnell; R J Bertelsen

doi:10.1111/cea.13055

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

N O Jõgi, C Svanes, S P Siiak, E Logan, J W Holloway, J Igland, A Johannessen, M Levin, F G Real, V Schlunssen, W G C Horsnell, R J Bertelsen

Microbiology and Infection

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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.

Original language	English
Pages (from-to)	66-77
Number of pages	12
Journal	Clinical and Experimental Allergy
Volume	48
Issue number	1
Early online date	12 Dec 2017
DOIs	https://doi.org/10.1111/cea.13055
Publication status	Published - 1 Jan 2018

Keywords

Journal Article
allergy
ascaris
asthma
ECRHS
helminths
IgG4
Norway
RHINESSA
Toxocara
zoonosis

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

@article{092b9ecb159842cca65fcc35f67de35c,

title = "Zoonotic helminth exposure and risk of allergic diseases: A study of two generations in Norway",

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 = "Journal Article, allergy , ascaris , asthma , ECRHS , helminths, IgG4 , Norway , RHINESSA , Toxocara , zoonosis",

author = "J{\~o}gi, {N O} and C Svanes and Siiak, {S P} and E Logan and Holloway, {J W} and J Igland and A Johannessen and M Levin and Real, {F G} and V Schlunssen and Horsnell, {W G C} and Bertelsen, {R J}",

note = "{\textcopyright} 2017 The Authors. Clinical & Experimental Allergy Published by John Wiley & Sons Ltd.",

year = "2018",

month = jan,

day = "1",

doi = "10.1111/cea.13055",

language = "English",

volume = "48",

pages = "66--77",

journal = "Clinical and Experimental Allergy ",

issn = "0954-7894",

publisher = "Wiley",

number = "1",

}

TY - JOUR

T1 - Zoonotic helminth exposure and risk of allergic diseases

T2 - A study of two generations in Norway

AU - Jõgi, N O

AU - Svanes, C

AU - Siiak, S P

AU - Logan, E

AU - Holloway, J W

AU - Igland, J

AU - Johannessen, A

AU - Levin, M

AU - Real, F G

AU - Schlunssen, V

AU - Horsnell, W G C

AU - Bertelsen, R J

PY - 2018/1/1

Y1 - 2018/1/1

N2 - 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.

AB - 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.

KW - Journal Article

KW - allergy

KW - ascaris

KW - asthma

KW - ECRHS

KW - helminths

KW - IgG4

KW - Norway

KW - RHINESSA

KW - Toxocara

KW - zoonosis

U2 - 10.1111/cea.13055

DO - 10.1111/cea.13055

M3 - Article

C2 - 29117468

SN - 0954-7894

VL - 48

SP - 66

EP - 77

JO - Clinical and Experimental Allergy

JF - Clinical and Experimental Allergy

IS - 1

ER -

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

Abstract

Keywords

UN SDGs

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