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

Zoonotic helminth exposure and risk of allergic diseases: a study of two generations in Norway
Zoonotic helminth exposure and risk of allergic diseases: a study of two generations in Norway
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 sensitisation, in two generations in Bergen, Norway.Methods:Serum levels of total IgG4, anti-Toxocara spp. IgG4 and Ascaris spp. IgG4 were established by ELISA in two 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]), hay fever (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.
0954-7894
66-77
Jõgi, Nils Oskar
bce12b83-b4fd-4cf0-9606-de40882df877
Svanes, Cecilie
4a547f80-e3d3-47b4-ae0a-2741ad93c629
Siiak, Silver Peeter
c8e1471c-bf39-4040-ae5f-4716d4e91ef2
Logan, Erin
68bc8f19-eb59-497d-bc1c-0a9563266aeb
Holloway, John W.
4bbd77e6-c095-445d-a36b-a50a72f6fe1a
Igland, Jannicke
517909fe-2701-4955-9c97-022436a2e1ee
Johannessen, Ane
aa3ea773-3c29-45bf-a81f-d6cba2444542
Levin, Michael
2be78359-2a08-4885-a83c-4f7a6d1de986
Real, Francisco Gomez
e73463eb-e232-4b11-a9b0-2eb47dcb1dee
Schlunssen, Vivi
730c0a72-038e-48c9-91be-4889157cc647
Horsnell, William G.C.
b490aa17-3f96-49d3-8b02-821bf14e2537
Bertelsen, Randi J.
b3f942fa-f7a5-4b26-a2c2-2d1d1b50e115
Jõgi, Nils Oskar
bce12b83-b4fd-4cf0-9606-de40882df877
Svanes, Cecilie
4a547f80-e3d3-47b4-ae0a-2741ad93c629
Siiak, Silver Peeter
c8e1471c-bf39-4040-ae5f-4716d4e91ef2
Logan, Erin
68bc8f19-eb59-497d-bc1c-0a9563266aeb
Holloway, John W.
4bbd77e6-c095-445d-a36b-a50a72f6fe1a
Igland, Jannicke
517909fe-2701-4955-9c97-022436a2e1ee
Johannessen, Ane
aa3ea773-3c29-45bf-a81f-d6cba2444542
Levin, Michael
2be78359-2a08-4885-a83c-4f7a6d1de986
Real, Francisco Gomez
e73463eb-e232-4b11-a9b0-2eb47dcb1dee
Schlunssen, Vivi
730c0a72-038e-48c9-91be-4889157cc647
Horsnell, William G.C.
b490aa17-3f96-49d3-8b02-821bf14e2537
Bertelsen, Randi J.
b3f942fa-f7a5-4b26-a2c2-2d1d1b50e115

Jõgi, Nils Oskar, Svanes, Cecilie, Siiak, Silver Peeter, Logan, Erin, Holloway, John W., Igland, Jannicke, Johannessen, Ane, Levin, Michael, Real, Francisco Gomez, Schlunssen, Vivi, Horsnell, William G.C. and Bertelsen, Randi J. (2018) Zoonotic helminth exposure and risk of allergic diseases: a study of two generations in Norway. Clinical & Experimental Allergy, 48 (1), 66-77. (doi:10.1111/cea.13055).

Record type: Article

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 sensitisation, in two generations in Bergen, Norway.Methods:Serum levels of total IgG4, anti-Toxocara spp. IgG4 and Ascaris spp. IgG4 were established by ELISA in two 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]), hay fever (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.

Text Jõgi NO et al CEA 2017 AAM - Accepted Manuscript
Restricted to Repository staff only until 8 November 2018.
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Accepted/In Press date: 27 October 2017
e-pub ahead of print date: 8 November 2017
Published date: 1 January 2018

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Local EPrints ID: 415603
URI: https://eprints.soton.ac.uk/id/eprint/415603
ISSN: 0954-7894
PURE UUID: 4432f002-514d-4313-99f2-2c98efafcb1e
ORCID for John W. Holloway: ORCID iD orcid.org/0000-0001-9998-0464

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Date deposited: 16 Nov 2017 17:30
Last modified: 06 Jun 2018 12:59

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Contributors

Author: Nils Oskar Jõgi
Author: Cecilie Svanes
Author: Silver Peeter Siiak
Author: Erin Logan
Author: Jannicke Igland
Author: Ane Johannessen
Author: Michael Levin
Author: Francisco Gomez Real
Author: Vivi Schlunssen
Author: William G.C. Horsnell
Author: Randi J. Bertelsen

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