Accepted: 29 January 2018

DOI: 10.1111/pai.12875

ORIGINAL ARTICLE

Eating fish and farm life reduce allergic rhinitis at the age of
twelve

Styliana Vasileiadou | Göran Wennergren  | Frida Strömberg Celind | Nils Åberg | 

Rolf Pettersson | Bernt Alm | Emma Goksör

Department of Paediatrics, University
of Gothenburg, Queen Silvia Children’s
Hospital, Gothenburg, Sweden
Correspondence
Emma Goksör, Department of Paediatrics,
University of Gothenburg, Queen Silvia
Children’s Hospital, Gothenburg, Sweden.
Email: emma.goksor@vgregion.se
Funding information
The work was supported by the Swedish
Government under the ALF agreement
between the Government and the County
Councils, which provides financial support
for medical research; the Research
Foundation of the Swedish Asthma and
Allergy Association; the Gothenburg
Masonic Order Orphanage Foundation; the
Health and Medical Care Committee of the
Regional Executive Board, Västra Götaland
Region, Sweden.
Abstract
Background: The prevalence of allergic rhinitis has increased, but the cause of this
rise is partly unknown. Our aim was to analyse the prevalence, risk factors, and pro-
tective factors for allergic rhinitis in 12-­year-­old Swedish children.
Methods: Data were collected from a prospective, longitudinal cohort study of chil-
dren born in western Sweden in 2003. The parents answered questionnaires when
the children were 6 months to 12 years. The response rate at 12 years was 76%
(3637/4777) of the questionnaires distributed.
Results: At the age of 12, 22% of children had allergic rhinitis and 57% were boys.
Mean age at onset was 7.8 years, and 55% reported their first symptoms after 8 years.
The most common trigger factors were pollen (85%), furry animals (34%), and house
dust mites (17%). A multivariate analysis showed that the adjusted odds ratios and
95% confidence intervals for the independent risk factors for allergic rhinitis at 12
were as follows: parental allergic rhinitis (2.32, 1.94-­2.77), doctor-­diagnosed food al-
lergy in the first year (1.75, 1.21-­2.52), eczema in the first year (1.61, 1.31-­1.97), and
male gender (1.25, 1.06-­1.47). Eating fish once a month or more at age of 12 months
reduced the risk of allergic rhinitis at 12 years of age (0.70, 0.50-­0.98) as did living on
a farm with farm animals at 4 years (0.51, 0.32-­0.84). Continuous farm living from age
4 to 12 seemed to drive the association.
Conclusions: Allergic rhinitis affected > 20% of 12-­year-­olds, but was lower in chil-
dren who ate fish at 12 months or grew up on a farm with farm animals.

KEYWORDS
allergic rhinitis, cohort study, farm animal, fish, protective factor, risk factor

1 |  I NTRO D U C TI O N
The increased prevalence of allergic rhinitis is well known and a
significant cause of morbidity in children and adolescents.1 Some
studies suggest that although the increase in asthma is levelling off,
2,3
allergic rhinitis continues to rise.
The reasons why atopic diseases have become so common re-
main partly unknown, but we do know that the underlying mecha-
nisms are complex interactions between genetic and environmental
factors. Studying the risk factors and protective factors associated
with allergic rhinitis could give us a better pathophysiological under-
standing of the disease and inform of preventative strategies.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in
any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2018 The Authors. Pediatric Allergy and Immunology Published by John Wiley & Sons Ltd.

Pediatr Allergy Immunol. 2018;1–7. wileyonlinelibrary.com/journal/pai  |  1

 |
2       VASILEIADOU et al.
Earlier studies carried out on our birth cohort found that intro-
ducing fish to a child’s diet at an early age reduced the risk of allergic
rhinitis at 4 years,4 while living with farm animals lowered the risk at
8 years of age.5 In contrast, receiving broad-­spectrum antibiotics in the
first week of life increased the risk of allergic rhinitis at 8 years of age.5
This study analysed the prevalence, risk factors and protective fac-
tors for allergic rhinitis in the same birth cohort at 12 years of age.
Our hypothesis was that early life environment, like living on a farm,
and diet, like fish consumption, affects the risk of allergic rhinitis at
12 years of age. The term “living on a farm” refers to farms with farm
animals.
2 |  M E TH O DS
2.1 | Study design and study population
Data were collected from a prospective, longitudinal cohort study of
children born in western Sweden in 2003. Fifty per cent (8176 infants)
of the birth cohort were randomly selected and were invited to par-
ticipate, and 5654 families entered the study. After written informed
consent, the parents completed questionnaires when the child was 6
and 12 months and 4, 8 and 12 years of age that were based on the
Swedish version of the International Study of Asthma and Allergies
in Childhood (ISAAC) questionnaire and the Swedish BAMSE ques-
tionnaire, which translates as Children, Allergy, Milieu, Stockholm,
Epidemiology. Details regarding the questionnaires and earlier re-
sponse rates have previously been published.4,5 At 12 years of age,
questionnaires were distributed to the families entering the study
(4777/5654), excluding those that had declared that they no longer
wished to participate. The response rate at 12 years of age was 76%
of the questionnaires distributed (3637/4777) and 64% of the families
entering the study (3637/5654). The study population for this study
was defined as those completing the questions regarding allergic rhi-
nitis at 12 years of age, that is 3618 families.
2.2 | Health outcomes and definitions
Breastfeeding duration and the age when various foods were intro-
duced were reported at 12 months. Parental allergic rhinitis, eczema
or asthma was defined as a parent reporting the specific allergic man-
ifestation ever. Frequent fish consumption during the first year of life
was defined as eating fish once a month or more, and farm living was
defined as living on a farm with farm animals and was asked at 4 years
and at 12 years of age. Continuously living on a farm was defined as
reported farm living at both ages. The question regarding farm living
did not specify what animals were kept on the farm, but refer to farm
animals such as cows, horses, pigs, hens, goats and sheep.
When the children were 8 and 12 years of age, we asked ques-
tions about their health and disease, allergy testing, family and
environment, including allergic rhinitis. Current allergic rhinitis was
defined as any reported symptoms of allergic rhinitis and medication
use during the last 12 months. Doctor-diagnosed allergic rhinitis was
reporting the medical diagnosis (ever) plus any symptoms of allergic
rhinitis or medication use during the last 12 months. The amount or
severity of symptoms was not specified.
The questions related to allergic rhinitis in the 12-­year question-
naire were as follows:
1. Has your child had symptoms of hay fever or allergic rhinitis
(sneezing, runny nose, blocked nose or red, itchy eyes) during
the last 12 months?
2. Has your child been diagnosed with hay fever or allergic rhinitis by
a doctor?
3. Has your child used medications for these disorders during the
last 12 months (tablets, nasal spray or eye drops)?
4. If your child has had allergic symptoms from the nose or eyes,
what has triggered this? Multiple answers were possible: cats,
dogs, horses, rodents, birch trees, grass, mugwort, house dust
mites or other allergens?
5. How many years old was your child when allergic rhinitis started?
Doctor-diagnosed asthma was parental reported doctor’s diagnosis
of asthma during the 12 first years (ever, but the question asked at
12 years) plus wheeze and asthma medication over the last 12 months
at 12 years. A doctor-diagnosed food allergy was parental reported
doctor’s diagnosis of food allergy during the 12 first years (ever) plus
any food allergic reaction to the food over the last 12 months at
12 years of age and a positive allergy test for the corresponding food.
Current eczema was based on reported current eczema over the past
12 months at 12 years of age and reported treatment with cortisone
cream for eczema over the past 12 months at 12 years of age.
A positive allergy test at 12 years was defined as reporting a pos-
itive allergy test, tested with skin prick test or blood test for specific
IgE. The test result was then specified for airborne (dog, cat, horse,
rabbit, house dust mites, timothy, birch, mugwort, mould) and/or
foods (egg, milk, fish, wheat, peanut, hazelnut, almond, other nuts,
soya, pea), with multiple answers possible.
2.3 | Statistics
The statistical analyses were performed using SPSS version 23 (IBM
Corp, Armonk, NY, USA), and we used frequencies, cross tabulations,
chi-­square and binary logistic regression. Odds ratios (OR) with 95%
confidence intervals (CI) were calculated, and a P-­value < .05 was
statistically significant.
The univariate statistical analysis was used to calculate the risk
for all potential risk factors or confounders for allergic rhinitis at
12 years of age.
The multivariate analysis included variables from birth until
12 months that had a univariate P-­value of < .1. These were as follows:
parental allergic rhinitis, eczema and asthma, gender, maternal med-
ication during pregnancy, having furry animals (dog, cat or rodent) at
home first year, fish and egg introduction before 9 months of age and
eating fish once a month or more, recurrent wheeze at 12 months of
age (> 3 episodes), eczema and a doctor-­diagnosed food allergy first
year. In addition, we asked about living on a farm at 4 years of age. We
VASILEIADOU et al.
also included factors that had previously been reported by studies to
affect the risk of allergic rhinitis and factors associated with socio-­
economic status, regardless of the level of significance. These were
smoking during pregnancy, parental education levels, short breast-
feeding duration, treatment with broad-­spectrum antibiotics during
the first week of life, being born small for gestational age and preterm
birth. Missing answers were coded as “missing.”
In addition, a multivariate model including all the variables men-
tioned above, with the only exception of farm living at 4 years, was
made to evaluate the possible impact of time of exposure, that is mov-
ing to or from a farm during childhood. In this model, farm living was
considered from age 4 to age 12 as never living on a farm, moved from
a farm (farm only at age 4), moved to a farm (farm only at age 12) and
continuously living on a farm (farm both age 4 and age 12).
Interaction analyses were performed for the independent fac-
tors in the multivariate analyses, using the binary logistic regression,
and considered significant if P < .05.
2.4 | Ethical approval
The Ethics Committee of the University of Gothenburg approved
the study, and all the parents provided written informed consent.
      3 |
doctor-­diagnosed allergic rhinitis at 12 years of age was 349 of 3618
(10%).
Two-­thirds of those with current allergic rhinitis only had that
condition at 12 years of age, while the other third had at least one
additional current atopic manifestation, namely asthma, eczema or
food allergies. The most prevalent current comorbidities at 12 years
were eczema (16%) and asthma (16%), with 6% reporting at least
2 comorbidities and 1% reporting three. Table 1 demonstrates the
gender distribution, prevalence of current additional allergic man-
ifestations at 12 years of age and heredity among those with, and
without, current allergic rhinitis.
Of the 805 children with current allergic rhinitis, 743 (92%) re-
ported at least 1 trigger factor: grass (68%), birch (60%), cats (28%),
mugwort (26%), house dust mites (18%), dogs (14%), horses (12%)
and rodents (8%). The combinations of various allergens are shown in
Figure 1.
The majority of the children with current allergic rhinitis, 450 of
805 (56%), reported allergy testing with a skin prick test, blood test
for specific IgE or both, with 85% reporting a positive result: 78%

3 | R E S U LT S

3.1 | Representativeness of the study sample

We analysed the differences between the children who participated
at 12 years of age and those who we had data from for the first
year of life. The children who did not take part at 12 years of age
were more likely to have parents with low education, mothers who
smoked during pregnancy and have been breastfed for < 4 months.
There also was a lower prevalence of atopic heredity among the non-­
participants (Table S1).

3.2 | Prevalence and clinical characteristics F I G U R E   1   Euler diagram of the prevalence of the trigger factors
for allergic rhinitis at 12 y of age: pollens, animals, house dust mites.
At the age of 12, 805 of 3618 (22%) children had current allergic rhi- The diagram illustrates the observed combinations of reported
nitis and 460 (57%) were boys (Table 1). The reported prevalence of triggers, and the areas are proportional to the number of children

TA B L E   1   Individuals with or without

Rhinitis % (n = 805) No rhinitis % (n = 2813) P-­value
current allergic rhinitis at 12 y of age, with
the prevalence of other current allergic Male gender 57 (460/804) 51 (1436/2810) .002
manifestations at 12 y of age, gender and Food allergy at 12 y of age 8 (65/803) 2 (44/2802) <.001
positive parental heredity for allergic
Eczema at 12 y of age 16 (131/802) 8 (229/2797) <.001
rhinitis, eczema and asthma
Asthma at 12 y of age 16 (121/774) 4 (110/2759) <.001
Wheeze at 12 y of age 19 (154/801) 5 (148/2801) <.001
Parental allergic rhinitis 61 (486/801) 36 (1003/2796) <.001
Parental eczema 47 (375/801) 36 (1007/2796) <.001
Parental asthma 23 (185/801) 14 (396/2796) <.001

The figures vary because of missing values. We present the actual percentages out of the number of
responses received, not the total cohort.
 |
4       VASILEIADOU et al.

TA B L E   2   Independent risk and

Variable aOR 95% CI
protective factors in the multivariate
Parental allergic rhinitis 2.32 1.94-­2.77 analysis for allergic rhinitis at 12 y of age
Doctor-­diagnosed food allergy first year 1.75 1.21-­2.52
Eczema first year 1.61 1.31-­1.97
Male gender 1.25 1.06-­1.47
Fish consumption ≥ 1×/month first year 0.70 0.50-­0.98
Living on a farm at age of 4 y 0.51 0.32-­0.84

aOR, adjusted odds ratio. The model was also adjusted for: maternal medication during pregnancy,
introduction of fish and introduction of eggs before 9 mo of age, recurrent wheeze at age 12 mo,
parental education, furry animals at home during the first year, breastfeeding for <4 mo, maternal
smoking during pregnancy, treatment with broad-­spectrum antibiotics during the first week of life,
being born small for gestational age, preterm birth < 37 wks, parental asthma and parental eczema.

reported IgE sensitization to airborne allergens and 30% to food al-

lergen. The three most common airborne allergens were birch (49%),
cats (42%) and timothy grass (38%).
Of the children with current allergic rhinitis, a parental history
of rhinoconjunctivitis was reported by 61%, eczema by 47% and
asthma by 23% (Table 1).

3.3 | Age of onset
In the 12-­year questionnaire, the mean reported age for the onset
of current allergic rhinitis was 7.8 years (median 9.0, range 0-­12).
Of the children with allergic rhinitis at the age of 12 years, 19%
reported allergic rhinitis for the first time in the 4-­year question-
naire, 27% for the first time in the 8-­year questionnaire and 55% for
the first time in the 12-­year questionnaire. Having an early onset
reported at 4 years was more common among boys, and associated
with other allergic manifestations at age 1 and age 4. In addition,
other allergic manifestations at 12 years of age and allergic rhinitis
triggered by birch, mugwort, horse or rodents were more common
among those with an early onset (data not shown). Of those report-
ing allergic rhinitis by the age of 4, 67% had persistent symptoms at
12 years of age. Persistent symptoms were more common among
those with eczema during infancy and a family history of atopy. In
addition, having allergic rhinitis triggered by birch at 4 years of age
was associated with persistent symptoms until 12 years of age (data
not shown).
3.4 | Univariate and multivariate analysis
The factors that demonstrated a significant association of P < .1 in
the univariate models are shown in Table S2.
In the multivariate analysis, a number of factors independently
increased the risk of current allergic rhinitis, namely parental allergic
rhinitis, doctor-­diagnosed food allergy in the first year of life, eczema
in the first year and male gender. In contrast, the risk was reduced
by eating fish once a month or more at 12 months and by living on
a farm (Table 2).
A third (33%) of the children who did not live on a farm, but had
a parental history of allergic rhinitis, also had allergic rhinitis. The
F I G U R E   2   Risk of current allergic rhinitis based on living on
a farm at 4 y of age and a parental history of allergic rhinitis,
presented as adjusted odds ratios and 95% confidence intervals.
The multivariate analysis was adjusted for the same factors as the
multivariate analysis presented in Table 2
figure for farm-­based children without a parental history of allergic
rhinitis was 8% (Figure S1). This result was supported by a multivar-
iate analysis that demonstrated that living on a farm at the age of
4 years reduced the risk of allergic rhinitis (Figure 2). This reduced
risk was still seen when the multivariate model (Table 2) was ad-
justed for reported sensitization at age 4, for avoiding furry animals
because of an allergy in the family and for the daily duration of out-
door activities.
In the multivariate analysis considering time of exposure, contin-
uously living on a farm (both at age 4 and age 12) was a statistically
significant protective factor for allergic rhinitis at 12 years of age
(Table 3).
3.5 | Stratified and interaction analyses
A stratified analysis based on the presence or absence of paren-
tal allergic rhinitis confirmed that eating fish once a month or
more had a significant protective effect in both groups (P = .03
and P < .001). In addition, the protective effect of living on a
farm was independent of parental allergic rhinitis (P = .049 and
P = .02).
There was no interaction between living on a farm and parental
history of allergic rhinitis (P = .87) or gender (P = .48) or eating fish
VASILEIADOU et al.
TA B L E   3   Prevalence of current allergic
rhinitis at 12 y of age (729/3276) based on
whether children lived on a farm at age of Never lived on a farm
4 and at 12 y of age Moved from a farm
Moved to a farm
Continuously lived on a
farm
Moved from a farm, farm only at age 4, moved to a farm, farm only at age 12 and continuously lived
on a farm, farm both at age of 4 and 12 y.
Farm living was defined as living on a farm with farm animals. To be included in the analysis, answers
on farm living at both ages were required. Odds ratios were adjusted (aOR) for all the factors in
Table 2 (multivariate analysis). Bold indicates statistical significance.
once a month or more (P = .59). Neither was there any significant
interaction between eating fish once a month or more and parental
history of allergic rhinitis (P = .15) or gender (P = .57).
4 | D I S CU S S I O N
In this prospective, longitudinal birth cohort study, we found that liv-
ing on a farm and early fish consumption reduced the risk of current al-
lergic rhinitis at 12 years of age. Furthermore, we were able to confirm
a high prevalence of current allergic rhinitis at 12 of age.
One in 5 children reported current allergic rhinitis, and pollen was
the most commonly reported trigger factor (Figure 1). This finding
agreed with the West Sweden Asthma Study, which stated that pollen
sensitization was strongly associated with rhinitis.6
Allergic rhinitis has been reported to become increasingly com-
mon as children grow into adolescence, with a stronger association
in males.7 This was supported by the findings in our study, which
showed a prevalence of 6% at 4 years of age, 11% at 8 years of age
and 22% at 12 years of age.4,5 The same prevalence was reported
8
in the BAMSE study at 12 years of age, and it was 18% at 11 years
of age in the Avon Longitudinal Study of Parents and Children.9 On
the other hand, some studies, like the UK Manchester Asthma and
Allergy Study and the Odense Adolescence Cohort Study on Atopic
Diseases and Dermatitis, reported a higher prevalence of above
9,10
30%. Different definitions of current allergic rhinitis can partly
account for these differences.
The development of atopy has been reported to be more pro-
11
nounced in children living in urban environments than on farms.
The lower risk of allergic rhinitis in children living on a farm in our
study supports this. Furthermore, the timing of exposure, with ex-
posure in early life having more effect, and the duration of exposure,
12
with a dose-­response effect, seems to be important. Some studies
have indicated that the protective effect of living on a farm in early
life continued into adulthood.13 In our study, it seemed to be the
continuous exposure, at both age 4 and age 12, that drove the neg-
ative association. This might indicate a dose-­response relationship;
that is, the longer the exposure, the stronger the protective effect.
No interaction was seen between farm living at preschool age and
heredity, and the protective effect of farm living was independent of
      5 |
Rhinitis % (n) No rhinitis % (n) aOR 95% CI
23 (692/3009) 77 (2317/3009) 1 Ref.
22 (10/46) 78 (36/46) 1.18 (0.57-­2.44)
21 (19/91) 79 (72/91) 1.03 (0.60-­1.77)
6 (8/130) 94 (122/130) 0.26 (0.13-0.55)
heredity in the multivariate analysis. It is also clear that the preva-
lence of allergic rhinitis was not due to underrepresentation of pa-
rental allergic heredity in children living on a farm.
Several independent microbial signals may play a role in activat-
ing the protective effects of living on a farm.14-16 One explanation
might be the stimulation of TH1 cells and suppression of TH2 cells
due to the increased exposure of farm children to microbial antigens
in stables or farmhouses.17
In addition, early dietary factors have been suggested to affect the
development of allergic disease.4,18-22 Our findings of that fish con-
sumption reduced the risk of allergic rhinitis agreed with such studies.
In a Norwegian birth cohort study, children who ate fish at an early age
displayed a lower prevalence of allergic rhinitis at 4 years of age.18 The
Stockholm BAMSE study found that early and regular fish consump-
tion in infancy was associated with a reduced risk of asthma, rhinitis
and eczema at 8 years of age.19 In addition, previous studies from our
cohort have concluded that the early introduction of fish reduced the
risk of eczema during the first year of life,20 allergic rhinitis and re-
current wheeze at 4 years of age 4,21 and doctor-­diagnosed asthma at
8 years of age.22
It has been suggested that the immunological effects of omega-­3
fatty acids, which are found in oily fish, explain how fish consumption
can reduce the risk of allergic diseases. 23,24 However, studies that
provided infants and children with omega-­3 fatty acid supplements
have reported inconsistent results. 25 Few epidemiological studies
have successfully distinguished oily and lean fish consumption in
childhood, and the results have been inconclusive. 20,26 Another hy-
pothesis is that other compounds than fatty acids in fish, including
certain vitamins or proteins, might have an impact on allergic dis-
ease. For example, vitamin D is found in fish and has been associated
with reduced allergy levels. 27-29 Moreover, regular fish consumption
might reflect living in a more positive socio-­economic environment
and a more healthy lifestyle in general.30
4.1 | Strengths and limitations
The main strengths of the study were the large size of the birth
cohort, the high response rate and the longitudinal design. In com-
mon with previous studies on this cohort, the material appears to be
largely representative of the population. 22
 |
6       VASILEIADOU et al.
A limitation that we shared with many other epidemiological stud-
ies was that the data collection was based on postal questionnaires.
To reduce the impact of this, we chose questions that were based
on previously used international questionnaires, as this enabled us
to compare the results. Our definition of “allergic rhinitis” included
both current medication use and current symptoms, even though the
amount or severity of symptoms was not specified. The reason not
to use a doctor’s diagnosis or sensitization is that many children in
Sweden use over-­the-­counter drugs without a doctor’s diagnosis to
alleviate symptoms of allergic rhinitis. Furthermore, questionnaire-­
based data on the results of clinical tests should be interpreted with
caution as parents may not remember or remember incorrectly. In
addition, an allergy test is not mandatory for the medical diagnosis of
allergic rhinitis given a typical medical history. Even so, the majority
of children with allergic rhinitis in our study reported allergy testing.
5 |  CO N C LU S I O N S
The latest stage of this birth cohort study of Swedish children found
that living with farm animals reduced the risk of allergic rhinitis at
12 years of age, as did eating fish once a month or more at the age of
12 months. Independent risk factors were parental allergic rhinitis, a
doctor-­diagnosed food allergy in the first year of life, eczema in the
first year of life and male gender.
ORCID
Göran Wennergren  http://orcid.org/0000-0002-7010-7191
Emma Goksör  http://orcid.org/0000-0001-9595-1877
REFERENCES
1. Mallol J, Crane J, von Mutius E, et al. The International Study of
Asthma and Allergies (ISAAC). Phase Three: a global synthesis.
Allergol Immunopathol (Madr). 2013;41:73‐85.
2. Bjerg A, Ekerljung L, Middelveld R, et al. Increased prevalence of
symptoms of rhinitis but not of asthma between 1990 and 2008 in
Swedish adults: comparisons of the ECRHS and GA²LEN surveys.
PLoS ONE. 2011;6:e16082.
3. Hicke-Roberts A, Åberg N, Wennergren G, Hesselmar B. Allergic
rhinoconjunctivitis continued to increase in Swedish children up to
2007, but asthma and eczema levelled off from 1991. Acta Paediatr.
2017;106:75‐80.
4. Alm B, Goksör E, Thengilsdottir H, et al. Early protective and risk
factors for allergic rhinitis at age 4½ yr. Pediatr Allergy Immunol.
2011;22:398‐404.
5. Alm B, Goksör E, Pettersson R, et al. Antibiotics in the first week of
life is a risk factor for allergic rhinitis at school age. Pediatr Allergy
Immunol. 2014;25:468‐472.
6. Bjerg A, Ekerljung L, Eriksson J, et al. Increase in pollen sensitization
in Swedish adults and protective effect of keeping animals in child-
hood. Clin Exp Allergy. 2016;46:1328‐1336.
7. Kurukulaaratchy RJ, Karmaus W, Raza A, Matthews S, Roberts
G, Arshad SH. The influence of gender and atopy on the natu-
ral history of rhinitis in the first 18 years of life. Clin Exp Allergy.
2011;41:851‐859.
8. Ballardini N, Kull I, Lind T, et al. Development and comorbidity of
eczema, asthma and rhinitis to age 12: data from the BAMSE birth
cohort. Allergy. 2012;67:537‐544.
9. Belgrave D, Granell R, Simpson A, et al. Developmental profiles of
eczema, wheeze, and rhinitis: two population-­based birth cohort
studies. PLoS Med. 2014;11:e1001748.
10. Christiansen ES, Kjaer HF, Eller E, et al. The prevalence of atopic
diseases and the patterns of sensitization in adolescence. Pediatr
Allergy Immunol. 2016;27:847‐853.
11. Braun-Fahrländer C, Gassner M, Grize L, et al. Prevalence of hay
fever and allergic sensitization in farmer’s children and their peers
living in the same rural community. SCARPOL team. Clin Exp Allergy.
1999;29:28‐34.
12. Riedler J, Braun-Fahrländer C, Eder W, et al. Exposure to farming in
early life and development of asthma and allergy: a cross-­sectional
survey. Lancet. 2001;358:1129‐1133.
13. Eriksson J, Ekerljung L, Lötvall J, et al. Growing up on a farm
leads to lifelong protection against allergic rhinitis. Allergy.
2010;65:1397‐1403.
14. von Ehrenstein OS, von Mutius E, Illi S, Baumann L, Böhm O, von
Kries R. Reduced risk of hay fever and asthma among children of
farmers. Clin Exp Allergy. 2000;30:187‐193.
15. Kilpeläinen M, Terho EO, Helenius H, Koskenvuo M. Farm environ-
ment in childhood prevents the development of allergies. Clin Exp
Allergy. 2000;30:201‐208.
16. Stein M, Hrusch C, Gozdz J, et al. Innate immunity and asthma risk in
Amish and Hutterite farm children. N Engl J Med. 2016;375:411‐421.
17. Riedler J, Eder W, Oberfeld G, Schreuer M. Austrian children living
on a farm have less hay fever, asthma and allergic sensitization. Clin
Exp Allergy. 2000;30:194‐200.
18. Nafstad P, Nystad W, Magnus P, Jaakkola JJ. Asthma and allergic
rhinitis at 4 years of age in relation to fish consumption in infancy. J
Asthma. 2003;40:343‐348.
19. Magnusson J, Kull I, Rosenlund H, et al. Fish consumption in infancy
and development of allergic disease up to age 12 y. Am J Clin Nutr.
2013;97:1324‐1330.
20. Alm B, Åberg N, Erdes L, et al. Early introduction of fish decreases
the risk of eczema in infants. Arch Dis Child. 2009;94:11‐15.
21. Goksör E, Alm B, Thengilsdottir H, Pettersson R, Åberg N,
Wennergren G. Preschool wheeze – impact of early fish introduc-
tion and neonatal antibiotics. Acta Paediatr. 2011;100:1561‐1566.
22. Goksör E, Alm B, Pettersson R, et al. Early fish introduction and
neonatal antibiotics affect the risk of asthma into school age.
Pediatr Allergy Immunol. 2013;24:339‐344.
23. Black PN, Sharpe S. Dietary fat and asthma: is there a connection?
Eur Respir J. 1997;10:6‐12.
24. Bisgaard H, Stokholm J, Chawes B, et al. Fish oil-­derived fatty acids
in pregnancy and wheeze and asthma in offspring. N Engl J Med.
2016;375:2530‐2539.
25. Kremmyda LS, Vlachava M, Noakes PS, Diaper ND, Miles EA, Calder
PC. Atopy risk in infants and children in relation to early exposure
to fish, oily fish, or long-­chain omega-­3 fatty acids: a systematic re-
view. Clin Rev Allergy Immunol. 2011;41:36‐66.
26. Øien T, Storrø O, Johnsen R. Do early intake of fish and fish oil pro-
tect against eczema and doctor-­diagnosed asthma at 2 years of age?
A cohort study. J Epidemiol Community Health. 2010;64:124‐129.
27. Mullins RJ, Camargo CA Jr. Shining a light on vitamin D and
its impact on the developing immune system. Clin Exp Allergy.
2011;41:766‐768.
28. Hollams E, Teo S, Kusel M, et al. Vitamin D over the first decade
and susceptibility to childhood allergy and asthma. J Allergy Clin
Immunol. 2017;139:472‐481.
29. Grant C, Crane J, Mitchell E, et al. Vitamin D supplementation during
pregnancy and infancy reduces aeroallergen sensitization: a ran-
domized controlled trial. J Allergy Clin Immunol. 2016;71:1325‐1334.
VASILEIADOU et al. |
      7

3 0. Almqvist C, Garden F, Xuan W, et al. Omega-­3 and omega-­6 fatty

acid exposure from early life does not affect atopy and asthma at How to cite this article: Vasileiadou S, Wennergren G,
age 5 years. J Allergy Clin Immunol. 2007;119:1438‐1444. Strömberg Celind F, et al. Eating fish and farm life reduce
allergic rhinitis at the age of twelve. Pediatr Allergy Immunol.
S U P P O R T I N G I N FO R M AT I O N 2018;00:1–7. https://doi.org/10.1111/pai.12875

Additional Supporting Information may be found online in the

­supporting information tab for this article.