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What effect does breastfeeding have on coeliac

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Therapeutics
Systematic review

What effect does breastfeeding have on coeliac

disease? A systematic review update
Camilla Henriksson,1 Anne-Marie Bostrm,2,3 Ingela E Wiklund4
10.1136/eb-2012-100607

1
Department of Biosciences and
Nutrition, Karolinska Institutet/
Stockholm University,
Stockholm, Sweden
2
Division of Nursing,
Department of Neurobiology,
Care Science and Society,
Karolinska Institutet, Stockholm,
Sweden
3
Department of Geriatric
Medicine, Danderyd Hospital,
Stockholm, Sweden
4
Division of Obstetrics and
Gynaecology, Department of
Clinical Sciences, Danderyd
Hospital, Karolinska Institutet,
Stockholm, Sweden
Accepted 8 July 2012

Correspondence to:
Dr Ingela E Wiklund
Department of Clinical Sciences,
Danderyd Hospital, Karolinska
Institutet, 182 88 Stockholm,
Sweden;
ingela.wiklund@bbstockholm.se

Abstract
Objective To update the evidence published in a previous
systematic review and meta-analysis that compared the
effect of breastfeeding on risk of coeliac disease (CD).
Material and methods A systematic review of observational studies published between 1966 and May 2004 on
the subject was conducted in 2005. This update is a systematic review of observational studies published
between June 2004 and April 2011. Pubmed, EMBASE
and Cinahl were searched for published studies that
examined the association between breastfeeding and CD.
Results After duplicates were removed 90 citations were
screened. Four observational studies were included in the
review. Two of three studies which had examined the
duration of breastfeeding and CD reported signicant
associations between longer duration of breastfeeding
and later onset of CD (OR ranged from 0.18 to 0.665).
Breastfeeding during the introduction of gluten to the
infant was reported to have a protective effect in two
studies.
Conclusions Our ndings support previous published
ndings that breastfeeding seems to offer a protection
against the development of CD in predisposed infants.
Breastfeeding at time of gluten introduction is the most signicant variable in reducing the risk. Timing of gluten
introduction may also be a factor in the development of CD.

Introduction
Coeliac disease (CD), also known as gluten sensitive
enteropathy, is a chronic autoimmune disease that affects
the small intestine in genetically predisposed individuals.
CD is induced by dietary intake of wheat gluten and
related prolamines, for example, in rye and barley. Most
of the individuals with CD carry a human leucocyte
antigen (HLA)-DQ2 or DQ8 haplotype gen but so does
about 30% of the general population.1 The prevalence of
CD is difcult to determine when the disease can be
asymptomatic for a long time and the diagnosed prevalence varies from 3 to 14 / 1000 children which means
that the environmental factors in the aetiology play a
crucial role.1 The disease is multifactorial and CD seems
to act as a combination of adaptive and innate immune
response to gluten. Studies show that one of the most
critical environmental factors is early infant feeding
practices with focus on breastfeeding.2 3
Breastfeeding is a subject for constant debate and
strong opinions, not whether or not it has positive
effects for the infant, but more as a question of how
good it is and for what. As early as in the 1950s, breastfeeding was suggested to have a protective effect and
that breastfed infants had a later onset of CD. For the
last decades epidemiological studies have shown

breastfeeding to be a crucial element in allergy development.4 The mechanisms underlying the aetiology are not
fully understood and therefore nor the mechanisms
behind the protective effect. Continuing breastfeeding at
time of gluten introduction has been suggested to limit
the amount of gluten the child receives and thereby
decreasing the chance of developing the symptoms of
CD. Another possible explanation is that the milk in
itself protects against gastrointestinal infections.2 4 Such
infections may lead to increased permeability which
allows gluten to pass on into the lamina propia triggering the process of CD in susceptible individuals.4
Whatever the mechanism might be, breastfeeding is the
most important environmental factor in CD development
for an infant. That makes this area of research important
since there are indications that breastfeeding rates are
declining. For example, in the Stockholm area in
Sweden the number of children exclusively breastfeeding have declined by 10.5% in the last 15 years, if this
has an effect on prevalence of CD is yet to be seen.5
The WHO declared in a systematic review from 2002
that one of their goals is that 80% of all the children in
the world should be exclusively breastfed for 6 months.6
Sweden and many other European countries adapted
this recommendation, which means that other foods,
such as wheat, should be introduced after 6 months.
Lately, it has been questioned whether this is the best
way of introducing possibly allergenic foods. Models in
animals suggest that oral tolerance is an allergen-driven
process and that there is a critical early window when
exposure to proteins is essential to the development of
this process.7 The timing for this window for oral allergen tolerance is not fully established in humans but
current studies point towards it being between 4 and
6 months.7 8 This makes the timing of gluten introduction and whether it is introduced under the protection
of breastfeeding or not a signicant question.
In 2005, Akobeng et al2 conducted a systematic
review and a meta-analysis with the aim to explore the
potential association between breastfeeding and reduced
risk of CD. The following outcomes were examined: (1)
the effect of breastfeeding compared with no breastfeeding; (2) the effect of duration of breastfeeding and (3)
the effect of breastfeeding at time of introduction of
dietary gluten. Akobeng et al2 systematically searched
various databases for studies examining these effects
published from 1966 to May 2004. The result of the
study suggested that breastfeeding may offer protection
against the development of CD. A meta-analysis of four
of the six studies indicated that children being breastfed
at the time of gluten introduction had a 52% reduction
in risk of developing CD compared with their peers who
were not breastfed at the time of gluten introduction.

Evidence-Based Medicine Month 2012 | volume 0 | number 0 |

Copyright Article author (or their employer) 2012. Produced by BMJ Publishing Group Ltd under licence.

Therapeutics
This study aims to update the evidence published in the
systematic review with articles published from June
2004 to April 2011 in order to evaluate possible developments in this research eld. Following research questions guided the study: (1) the effect of breastfeeding
compared with no breastfeeding; (2) the effect of duration of breastfeeding and (3) the effect of breastfeeding
at the time of introduction of dietary gluten.

Material and methods

In this review we have used similar review methodology
(types of studies, search strategy and assessments) and
examined the identical outcomes as in the previous published systematic review.2

Data extraction
Information and data on relevant features and results
was extracted from each of the included studies. When
data was missing or unclear in the published paper we
emailed the authors for more information. None of the
authors responded on our requests.
Data analysis
In the included studies many different assessments for
breastfeeding and statistical tests were used, and the
presentation of data prevented us from performing a
meta-analysis. Therefore, the ndings from the articles
are presented in narrative form.

Results
Types of studies
Included studies were observational studies and one
casecontrol study with the same inclusion criteria as in
the systematic review: (1) compared risk of CD in people
who were breastfed with risk in those who were not
breastfed, or compared risk of CD according to duration
of breastfeeding; (2) had used histological criteria for
diagnosing CD; (3) had controlled for potential confounders by matching in the study design or used risk
adjustment in the analysis and (4) had provided sufcient data to allow the reconstruction of 2 2 tables to
determine relative risks or OR with 95% CI. Only articles
written in English were included.
Search strategy
Pubmed, EMBASE and Cinahl were systematically
searched for articles and studies published between June
2004 and April 2011 with the search strategy presented
in table 1. The search was conducted on 25 April 2011.
The reference lists of the relevant citations found in this
search was examined for further potentially appropriate
articles.
Assessment of study eligibility
The rst author assessed each article for eligibility using
the inclusion criteria above. Unclear citations were discussed with the other authors and agreement reached by
consensus.
Assessment of methodological quality
The authors independently rated methodological quality
of selected studies using the Critical Appraisal Skills
Programme (Oxford, UK) tool for observational studies.9
Each study was grade as A (low risk of bias), B (moderate
risk of bias) or C (high risk of bias) according to published
criteria.10 Disagreements were resolved by consensus.

Table 1 Search strategy

Coeliac disease OR Celiac disease OR Gluten sensitive

enteropathy OR sprue

Celiac disease [MESH]

1 OR 2

Breast feeding OR Breastfeeding OR Breast-feeding

Breast feeding [MESH]

4 OR 5

3 AND 6

Evidence-Based Medicine Month 2012 | volume 0 | number 0 |

Description of included studies

The initial search resulted in 164 identied records; after
duplicates were removed 90 records remained. After
reading the abstracts we excluded articles not focusing
on the association of breastfeeding and the development
of CD. Articles not written in English were also excluded
together with articles in the form of comment and
reviews. Of these 90 records only 10 were identied as
potentially relevant studies (gure 1). Six were excluded
for following reasons. Four were review articles and did
not report original data.4 8 11 12 One did not conrm CD
in a correct way13 and one was an animal study.14 One
citation was an abstract in a conference report,15
although the results from this abstract will be included
in the update. Thus, four studies were identied that met
the inclusion criteria.1518 Three studies were observational studies1618 and one a casecontrol study.15 They
were originated in different countries, one in Serbia,16
two in the USA17 18 and one in Spain.15 They ranged
from 8916 to 173715 participants of varying age.
Description of included studies is presented in table 2.
No cohort study was found on the subject. All participants had been diagnosed to have CD based on small
intestinal biopsy. All studies used questionnaires or
interviewing techniques to obtain infant feeding history
from parents.
Methodological quality of included studies
The methodological quality of each study was evaluated
and a summary of the methodological quality and the
grades are shown in table 2.
Association between breastfeeding and coeliac disease
Ever breastfed versus never breastfed
No study was conducted with children who had never
been breastfed therefore no comparisons of the groups
based on this variable could be conducted.
Duration of breastfeeding
Radlovic et al16 did a retrospective observational study
of 89 infants with CD using their medical records to
determine the duration of breastfeeding and timing of
gluten introduction at the University Childrens Hospital
in Belgrade. The infants were divided into one group
that had been exclusively breastfed at the time of gluten
introduction (n=33) and a group that had not been
breastfed at the time of gluten introduction (n=56). The
infants were also divided into groups based on the

Therapeutics

Figure 1

Flowchart of selection of the included studies based on Prisma 2009 Flow Diagram.

timing of gluten introduction: prior to the fourth month

(n=22), between the fourth and sixth month (n=36) and
after the sixth month (n=4). The researchers conducted a
conditional logistic regression to estimate the impact of
early feeding practices, that is, duration of breastfeeding,
timing of gluten introduction and breastfeeding at the
time of gluten introduction on the risk of disease onset
in the rst year of life. The results revealed that longer
duration of breastfeeding signicantly reduced the risk
to develop CD in the rst year of life (OR 0.665; 95% CI
0.481 to 0.891) and the duration of breastfeeding was
the only signicant variable in delaying the age at the

CD diagnosis for this group of infants (B=0.49;

SE=0.159; p=0.007).
DAmico et al17 conducted a retrospective study with
141 children 20 years of age or less with CD and compared infants who where exclusively breastfed (n=40)
for at least 6 months with all other infants where the
vast majority was both breastfed and bottle fed (n=101).
The researchers showed that children who were exclusively breastfed in the rst 6 months developed symptoms signicantly later (on average 15 months later;
p<0.05) and were diagnosed with CD signicantly later
(at a mean age of 4 years and 10 month versus 2 years

Evidence-Based Medicine Month 2012 | volume 0 | number 0 |

Therapeutics
Table 2 Methodology of included studies (summary)
Confounding
factors
considered

Sample
size

Retrospectively
analysed
medical records

Age, sex

89 cases

724 months,
median
14 months

Within
cohort

Questionnaire

Age, sex

141 cases

8.4 years

Children with
CD, Denver
metropolitan
area

All
CD-negative
children in
cohort

Interview,
questionnaire

Ethnicity,
infant diet
choices

51 cases,
1509
controls

4.7 years

All new
CD-cases
2006-06
2007-05, 39
hospitals,
Spain

Children
paired for
age and sex

Questionnaire

993
cases,
744
controls

3.7 years

Not assessed

Reference
(country)

Case
selection

Control
selection

Exposure
measurement

Radlovic
et al
(Serbia)

Children with
coeliac
disease (CD),
UniChildrens
hospital,
Belgrade

Within
cohort

DAmico
et al (the
USA)

Children
under age 20
with CD, 30
different
states, USA

Norris
et al (the
USA)
Roman*
(Spain)

Age

Methodological
quality

*A conference report whose abstract was published but not yet the whole study.
A, low risk of bias; B, moderate risk of bias; C, high risk of bias.

and 11 months; p<0.05) than the other children.

Exclusively breastfeeding signicantly delayed the onset
of the symptoms leading to CD (OR 0.18, 95% CI 0.05 to
0.64). The study also showed that the exclusively breastfed children had lower rates of severe CD symptoms
( p<0.05).
Norris et al18 conducted a 10-year (19942004) prospective observational study in Denver, USA where 1560
children at increased risk for CD participated and 51
developed CD. The 51 children diagnosed with CD were
breastfed on average 8.3 (SD 8.8) months compared with
the other children who were breastfed 6.7 (SD 6.8)
months. No signicant difference was found between
the groups.
Roman15 conducted a nationwide prospective case
control study in Spain including 993 children with CD
and 744 paired controls from June 2006 to May 2007.
However, Roman did not report any results on this
outcome.

to sixth month. Results also showed a marginally

increased risk when gluten was not introduced until the
seventh month or later compared with those exposed at
46 months.
Roman15 reported that if gluten was introduced
while the child was still breastfeeding the risk of developing CD was reduced by 5862%. These results were
presented in a conference in June 2010 but the study
has not been published. This was the only casecontrol
study in the update.
To summarise our ndings, two of the three studies
which had examined the duration of breastfeeding and
CD reported signicant associations between longer duration of breastfeeding and later onset of CD.
Furthermore, three of the included four studies reported
that breastfeeding during gluten introduction signicantly delayed the onset of CD. Norris et al18 report that
timing of introduction of gluten into the infant diet is
signicantly associated with the appearance of CD.

Breastfeeding at the time of gluten introduction

Radlovic et al16 found that the 33 infants who had been
breastfed at the time for the gluten introduction were
signicantly older when diagnosed (mean=16.21
3.31 months) compared with the 56 infants who had
not been breastfed (mean=13.045.01 months; p=0.029).
DAmico et al17 did not report results on this
outcome.
Norris et al18 did not nd a signicant difference
between the children who were breastfed when rst
exposed to wheat, barley or rye with those who were not
breastfed. Of the 51 CD children, 49% were breastfed at
the time of gluten introduction versus 44% among the
1509 children without CD. The researchers showed
however that children exposed to gluten in the rst
3 months of life had a vefold increased risk compared
with children who were given gluten between the fourth

Discussion

Evidence-Based Medicine Month 2012 | volume 0 | number 0 |

The aim of this study was to update the previous published evidence in a systematic review and meta-analysis
examining the association between breastfeeding and
reduced risk of CD.2 The review suggested that breastfeeding may offer protection against the development of
CD and that children being breastfed at time gluten
introduction had a 52% reduction in risk of developing
CD compared with their peers who were not breastfed at
the time of gluten introduction.2 In this updated article
the results point in the same direction although the evidence is weaker. In the original review2 all included
studies were casecontrol studies, and in this update
only one casecontrol study was available. The remaining studies were observational studies reporting data in
various ways preventing us conducting a meta-analysis.
During the last 7 years there has been few studies

Therapeutics
conducted in this research eld which prevent a reliable
update of the meta-analysis. Two review articles
(although not systematic reviews) have been recently
published in support of our ndings; Silano et al8 conrms a negative correlation between the duration of
lu
breastfeeding and development of CD and Selimog
et al4 states that the most important preventive strategies
include the encouragement of breastfeeding. Our ndings in combination with the previous ndings from
Akobeng et als2 systematic review and the two recent
published review articles make its safe to say that
breastfeeding have an important role in delaying and/or
preventing the development of CD.
The ndings on timing of gluten introduction and
the circumstances at this point is also crucial. It is not
clear from these results (or previous ones) if breastfeeding provides a permanent effect against CD or if it
delays the symptoms. One study found no correlation
neither between the duration of breastfeeding nor if
gluten was introduced under the protection of breastfeeding.18 This study had relatively few cases (children
with CD; n=51) and this may explain why no correlation
was identied. The cases in this study were recruited
from a large birth cohort in Denver, Colorado, USA.
Cord blood samples were collected and screened and
infants with a specic HLA genotype was invited to participate. This means that these children and their parents
were selected because of their high risk of developing
autoimmune diseases such as CD. No dietary advice was
given to these families but it is impossible to rule out
that this did not affect the choice of infant diet. It was a
prospective observational study and recall bias is therefore a minimal risk.
Breastfeeding, infant feeding, weaning and everything related to it are subjects where everyone has an
opinion and where medical facts are combined with traditions. There are national differences as well as cultural
and personal beliefs between how parents choose to
feed their children. In the previous systematic review the
study objects originate from three different countries;
Italy, Germany and Sweden.2 In this update the included
studies are conducted in three other countries; Serbia,
the USA and Spain. Together these six countries represent widely shifting prevalence of breastfeeding with
Italy and Serbia with the lowest percentage were only
18% and 23% of the infants are breastfeeding at
4 month and with Sweden in the top where practically
all children are breastfed during the rst week and 60%
still at 4 months of age. USA and Spain are somewhere
in-between with rates at 33% and 40% at 4 months.19 20
Despite these differences nearly all studies have the
same results; when it comes to CD, breastfeeding seems
to have a protective effect against the development. The
previously published evidence are conrmed and reinforced by the new ndings in this update and one could
assume that future studies will continue to conrm this
nding.
Sweden is a country with one of the highest rates of
breastfeeding in the world; however, the rates are dropping. In a report from 2010 conducted in the Stockholm
area results showed that breastfeeding rates are declining
at both 4 months as well as the share of infants being
breastfed at age 1 week.5 The reason for this decline is

probably multifactorial. But what is interesting is what

effect the decreasing breastfeeding rate will have on CD
prevalence. In a study with the aim to use a statistical
method in order to calculate a risk factor over a time
period the association between breastfeeding and CD
among the 596 122 babies born in England and Wales
was examined. It was found that CD could be prevented
over 79 years if no breastfeeding as a risk factor was
eliminated. The number of cases that could be prevented
was 2655 (95% CI 1937 to 3343).21 If we interpret the
results of this review and previous studies the prevalence
of the disease may increase with higher cost for the individual family and the healthcare system. In Sweden the
National Food Administration (NFA) is responsible for
diet recommendations for the whole population, including infants.22 Since WHO in 2002 declared its policy to
recommend 6 months exclusive breastfeeding NFA has
made the same recommendations. As aforementioned,
this has been questioned in relation to food allergy and
in May 2011 NFA announced in a press release that the
infant feeding recommendations are under consideration
and will be updated during the year. Norris et al18
showed that timing of gluten introduction was associated with the appearance of CD with an increased risk
if introduced in the rst 3 months or in the seventh or
later. European Food Safety Association and European
Society for Paediatric Gastroenterology, Hepatology and
Nutrition recommends introduction of wheat not earlier
than 4 months and no later than 6 months to reduce the
risk of CD.23 However, NFA and its European counterparts stress the importance of gluten being introduced
while the infant is still breastfeeding.
Method discussion
We chose to expand the inclusion criteria with the
knowledge that the studies would not be totally equivalent to the ones in the rst systematic review and
meta-analysis. Both the outcome and the exposure were
dened differently in the separate studies and the results
could not be pooled together. A golden standard is
missing for how to dene and report exclusive and
partial breastfeeding just like there is a clear denition
of the CD diagnosis. In different countries and cultures
infant feeding is thought of in different ways. This could
be depending on everything from duration of maternity
leave to traditions passed on from generation to generation regarding opinions about optimal nutrition.
Limitations
The results of this review are subject to limitations.
Akobeng et al conducted their search in May 2005 and we
performed our search 6 years later but only four new
studies were found. The two of the four studies were
assessed to be of moderate risk of bias (grade B) and one
study was assessed to be of high risk of bias. Two-included
studies used retrospective design which is subject to recall
bias. Using interviews and questionnaires, as done in most
of these studies, misclassication of infant feeding is
likely to occur, both of duration of breastfeeding and age
of introduction of gluten. Such misclassication severely
affects the results. Retrospective observational studies as a
method is always in risk of bias with the consequence that
other risk factors could be less countered for. None of the

Evidence-Based Medicine Month 2012 | volume 0 | number 0 |

Therapeutics
included studies accounted for socioeconomic status to be
a confounding factor although this is a crucial factor for
diet choice. Furthermore, the published studies provided
only data for narrative presentation and we could not
conduct a meta-analysis. Thus, the ndings from this
updated review must be interpreted with caution.

Conclusions and future research

Breastfeeding seems to offer a protection against the
development of CD in predisposed infants. Breastfeeding
at time of gluten introduction and the total duration of
breastfeeding appears to be the two most signicant
variables in reducing the risk. Timing of gluten introduction may also be a factor in the development of CD.
Whether possibly allergenic food should be introduced
during a critical early window or not is a subject for
future research.

Competing interests None.

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