Pediatr Allergy Immunol 2008: 19: 375–380 Ó 2008 The Authors

DOI: 10.1111/j.1399-3038.2008.00718.x Journal compilation Ó 2008 Blackwell Munksgaard

PEDIATRIC ALLERGY AND

IMMUNOLOGY
Discussion Paper

The importance of early complementary

feeding in the development of oral tolerance:
Concerns and controversies
Prescott SL, Smith P, Tang M, Palmer DJ, Sinn J, Huntley SJ,
Cormack B, Heine RG, Gibson RA, Makrides M. The importance of
early complementary feeding in the development of oral tolerance:
Concerns and controversies.
Pediatr Allergy Immunol 2008: 19: 375–380.
Ó 2008 The Authors
Journal compilation Ó 2008 Blackwell Munksgaard
Rising rates of food allergies in early childhood reflect increasing failure
of early immune tolerance mechanisms. There is mounting concern that
the current recommended practice of delaying complementary foods
until 6 months of age may increase, rather than decrease, the risk of
immune disorders. Tolerance to food allergens appears to be driven by
regular, early exposure to these proteins during a Ôcritical early windowÕ
of development. Although the timing of this window is not clear in
humans, current evidence suggests that this is most likely to be between
4 and 6 months of life and that delayed exposure beyond this period
may increase the risk of food allergy, coeliac disease and islet cell
autoimmunity. There is also evidence that other factors such as
favourable colonization and continued breastfeeding promote tolerance
and have protective effects during this period when complementary
feeding is initiated. This discussion paper explores the basis for concern
over the current recommendation to delay complementary foods as an
approach to preventing allergic disease. It will also examine the growing
case for introducing complementary foods from around 4 months of
age and maintaining breastfeeding during this early feeding period, for
at least 6 months if possible.
Susan L. Prescott1, Peter Smith2, Mimi
Tang3, Debra J. Palmer4, John Sinn5,
Sophie J. Huntley6, Barbara
Cormack7, Ralf G. Heine8, Robert
A. Gibson9 and Maria Makrides4
1
School of Paediatrics and Child Health Research,
University of Western Australia, Perth, WA, 2Bond
University Medical School, Gold Coast, Qld,
3
Department of Allergy and Immunology, Royal
ChildrenÕs Hospital, Parkville, Vic., 4WomenÕs and
ChildrenÕs Health Research Institute, Children, Youth
and WomenÕs Health Service, Adelaide, SA,
5
Department of Neonatology, Royal North Shore
Hospital, St Leonards, NSW, 6Department of
Nutrition and Dietetics, Flinders University, Adelaide,
SA, Australia, 7Nutrition Services, Auckland City
Hospital, Auckland, New Zealand, 8Department of
Gastroenterology and Clinical Nutrition, Royal
ChildrenÕs Hospital, Parkville, Vic., 9School of
Agriculture, Food and Wine, The University of
Adelaide, Adelaide, SA, Australia
Key words: infant feeding; weaning practices; allergy
prevention; growth and development
Prof. Susan L. Prescott, School of Paediatrics and
Child Health Research, University of Western
Australia, Princess Margaret Hospital, PO Box D184,
Perth, WA 6001, Australia
Tel.: +61 8 9340 8171
Fax: +61 8 9388 2097
E-mail: sprescott@meddent.uwa.edu.au

Accepted 9 January 2008

There has been a clear and worrying increase in a
diverse range of allergic and autoimmune diseases,
which are all associated with an underlying failure
of immune tolerance (to allergens and self-anti-
gens). This emphasizes the need to understand the
developmental origins of these conditions and, in
particular, the role of early feeding practices in
both pathogenesis and prevention.
In 2001, the World Health Organisation
(WHO) revised its recommendation for exclusive
breastfeeding from 4 to 6 months (1). This was
based (at least in part) on reduced gastrointesti-
nal infectious disease noted in a Belarussian
study (2), and had major implications for disease
burden in developing and semi-industrialized
countries. At that time, there was also a paucity
of evidence regarding the other risks and benefits
of introducing complementary foods from 4 vs.
6 months of age (1). These recommendations
were aimed at reducing morbidity in developing
countries, but may not be appropriate in the
growing world population experiencing progres-
sive industrialization and escalating risk of
immune dysregulation.
Similar recommendations have been adopted
for the prevention of allergic disease in the USA,
375
Prescott et al.
the UK, Australia and other industralized
countries, based on the theoretical concern for
increased gut permeability and immaturity of
mucosal immunity in infants. However, there is
now mounting concern and some new evidence
that this recommendation for delayed introduc-
tion of complementary foods may have detri-
mental consequences. In Western countries,
where these recommendations have been adopted
into practice, rates of food allergy have escalated
rather than declined in the last 10 yr (3–5). The
purpose of this discussion paper is to highlight
these concerns and controversies (in term in-
fants), together with the rationale for revising
guidelines to more accurately reflect current
evidence, at least until more definitive studies
can be performed.
Implication for immune tolerance
Development of immune tolerance is a critical
process in early life. The rising rates of allergic
and autoimmune diseases highlight the suscepti-
bility of these tolerance pathways to environ-
mental changes. Although the mechanisms are
not clear, many of these conditions (including
food allergies, coeliac disease and type 1 diabe-
tes) manifest early in life, indicating that immune
dysregulation is a very early event. Animal
models suggest that tolerance is an antigen
(allergen)-driven process and that exposure to
these proteins during a Ôcritical early windowÕ of
development may be essential to this process
(Fig. 1). This also appears to coincide with the
establishment of healthy gut colonization, which
has been shown to be essential in promoting
tolerance to both allergens and self antigens (6).
Delays in either colonization (6) or antigen/
allergen exposure (7, 8) can lead to failure of oral
tolerance. Conversely, allergen exposure too
risk window risk
Tolerance
induction
Birth 3–4? 6–7?
? ?
Factors that influence the capacity for tolerance:
• optimal colonisation
• genetic pre-disposition
• allergen properties (dose, interval, timing, preparation)
• gut permeability/maturity/pH
• continued breast feeding?
• other immunomodulatory factors (fatty acids? stress? antioxidants?)
Fig. 1. Possible Ôwindow of toleranceÕ for introduction of
complementary foods.
376
early when the gut colonization and local
immune networks are less established may
increase the risk of allergic or autoimmune
disease (possibly through increased gut perme-
ability) (9). Some studies also suggest that
continued breastfeeding during introduction of
complementary foods is important for promoting
tolerance (10). The timing of this Ôcritical win-
dowÕ for oral allergen exposure is not clear in
humans, but current evidence suggests that this
may be between 4 and 6 months of life, as
discussed below. This raises further concerns
over recommendations for delaying introduc-
tions of complementary foods until after
6 months of age (1, 11), especially in industrial-
ized countries where the incidence of allergy is
high. It may be further argued that infants with a
genetic predisposition to allergic disease (failure
of oral tolerance) may require regular, larger
ÔdosesÕ of food allergen to promote tolerance
induction (as with immunotherapy). If this is the
case, allergen avoidance is likely to be detrimen-
tal in these children. However, at this stage this is
not known.
The basis and evolution of current recommendations for
infant feeding in allergy prevention
In the last 25 yr, observational and primary
allergy prevention studies in allergy with respect
to the early introduction of complementary foods
have been inconclusive, and at best, several
studies demonstrate a transient increase in IgE,
particularly to milk if foods were introduced
before 3–4 months of age. Here, we explore the
historical basis for current recommendations:
In the 1980s and 1990s, several studies
reported an association between early introduc-
tion of solids (<3–4 months) and eczema
(12)14). This association did not persist beyond
12 months of age in two of these three cohorts
(18, 19). A number of subsequent prospective
studies have failed to demonstrate an association
resolution between early introduction of complementary
foods and either eczema or food allergy, and a
recent systematic review concluded that there
was Ôno strong evidence to support the associa-
>12 months
tion between early solid feeding and the devel-
opment of persistent asthma, persistent food
allergy, allergic rhinitis, or animal dander allergyÕ
(17).
Despite the paucity of clear evidence, conser-
vative avoidance recommendations remain in
place in many countries. These appear to be
based on an early US study by Zeiger and Heller
(18), which used combined dietary avoidance
strategies in infants at risk of allergic disease.
 Early complementary feeding in the development of oral tolerance
Strategies included maternal allergen avoidance
(in pregnancy and lactation), extensively hydro-
lysed formula if complementary feeding was
required in the first year, and staged delay in
introduction of solid foods: non-legume vegeta-
bles, rice cereal, meats and non-citrus fruits
between 6 and 12 months; cowÕs milk, wheat,
soy, corn and citrus fruits between 12 and
18 months; eggs at 24 months; and peanut and
fish at 36 months. The main findings of these
studies were as follows.
(i) Reduction in food-associated atopic derma-
titis, urticaria and/or gastrointestinal disease
by 12 months (5.1% vs. 16.4%; p = 0.007).
This was only significant with a grouped
symptom analysis.
(ii) In the prophylaxis (treated) group, there was
a lower rate of sensitization to foods at
24 months (16.5% vs. 29.4%; p = 0.019),
due mainly to fewer positive milk skin tests
(1% vs. 12.4%; p = 0.001).
(iii) Serum IgE levels in the prophylaxis group
were marginally lower only at 4 months.
These findings could also be attributed to the
use of an extensively hydrolysed formula.
Despite this, the entire infant weaning structure
of this study has been incorporated into the
recommendations of the Committee on Nutri-
tion of the American Academy of Pediatrics in
2000 (19) and recently reinforced by a position
paper from the American College of Asthma
Allergy and Immunology (20). These avoidance
recommendations have been presented at many
international meetings and propagated by pro-
fessional societies and government agencies to
the wider community. The European Society
for Paediatric Allergology and Clinical Immu-
nology Committee on Hypoallergenic Formulas
and the European Society for Paediatric
Gastroenterology, Hepatology and Nutrition
(ESPGHAN) have been more circumspect,
suggesting the introduction of solids after
5 months (21).
In summary, the evidence for restricting
infant diet (complementary foods) for up to
6 months is weak, comprising inconsistent find-
ings of increased milk sensitization and eczema
with complementary foods given in the first
3–4 months.
Summary of current guidelines for allergy prevention
In 2005, we (Prescott and Tang) revised the
Australian allergy prevention guidelines, remov-
ing the inhalant avoidance strategies in light of
weak evidence and paradoxical effects in some
studies (11). We also raised concerns about the
lack of good evidence to support many food
allergen avoidance practices (some of which
avoid ÔallergenicÕ foods such as egg and peanuts
for between 2 and 4 yr of age). As indicated
above, any benefit of early food allergen avoid-
ance appears to be largely in the first
3–4 months, with very little clear or consistent
evidence that avoidance beyond this period
reduces allergy risk. Therefore, in the context
of allergy prevention, we elected to maintain
the previous recommended duration of exclu-
sive breastfeeding at Ô4–6 monthsÕ [consistent
with the ESPGHAN recommendations of
5 months (21)], despite the WHO recommen-
dations (1) for exclusive breastfeeding of all
infants for Ôat least 6 monthsÕ. Moreover, based
on the current evidence (presented below), there
may now be a case for revising this further to
Ô4 monthsÕ. Although the specific role in allergy
prevention remains unclear, there is some
evidence that continued breastfeeding while
new foods are introduced is beneficial (10).
When breastfeeding is not possible, the use of
hydrolysed formulas appears to confer some
protective effect compared with normal cow
milk-based formulas and these are still recom-
mended, although it is generally recognized that
more studies are needed and the protective
effects are not great. Thus, until more data are
available, it is difficult to justify the restriction
of complementary foods until 6 months of age,
particularly in industrialized countries.
Rationale for reconsidering the role of early food
allergen exposure
The normal development of oral tolerance is an
antigen-driven process and may logically depend
on regular exposure to foods and other antigens
during a critical early window. These processes
are also likely to depend on other conducive
exposures [such as favourable gut colonization
(6), breast milk (10) and/or other nutritional
immunomodulatory factors]. It is now increas-
ingly evident that allergen exposure is not the
primary cause of the allergy epidemic, and that
allergen avoidance may be unsuccessful, or even
detrimental in allergy prevention. Indeed,
although rising rates of immune disease are likely
to reflect a combination of many environmental
changes that compromise tolerance, the intro-
duction of complementary foods must be con-
sidered in this complex modern context.
Understanding other early host–environment
interactions is essential to this.
377
Prescott et al.
Evidence to support a role of earlier exposure to food
proteins in immune tolerance
A number of recent studies suggest that exposure
to specific foods in the 4–6 months age range
may reduce the risk of food allergies (7) and
autoimmunity (8, 22) compared with children
first exposed either before or after this ÔwindowÕ.
Specifically, children initially exposed to cere-
als between ages 0 and 3 months [hazard ratio
(HR), 4.32; 95% confidence interval (CI), 2.0–
9.35] and those who were exposed after 6 months
(HR, 5.36; 95% CI, 2.08–13.8) had increased risk
of islet cell autoantibodies than those who were
exposed between 4 and 6 months (22). Similarly,
delayed exposure to gluten (after 6 months) was
associated with increased risk of coeliac disease
autoimmunity (HR, 1.87; 95% CI, 0.97–3.60)
and biopsy-diagnosed coeliac disease (HR, 3.98;
95% CI, 1.18–13.46; p = 0.04) compared with
those exposed at 4–6 months (8). Exposure prior
to 4 months was also associated with increased
risk of coeliac disease autoimmunity (HR, 5.17;
95% CI, 1.44–18.57) and biopsy-diagnosed coe-
liac disease (HR, 22.97; 95% CI, 4.55–115.93;
p = 0.001).
Although early allergic disease outcomes are
reduced in children who have not been exposed
to complementary foods prior to 4 months (12–
14, 23), there is little evidence that avoidance
beyond 4 months is beneficial (24). Moreover,
avoidance beyond 6 months has been associated
with increased risk of allergic disease (food
allergy, eczema, asthma) (7, 24). One recent
Australian study (in which reverse causation was
excluded) showed that even delaying comple-
mentary foods until after 3 months was associ-
ated with an increased risk of atopy at 5 yr of age
(25).
Intervention studies that have used infant
dietary avoidance strategies for allergy preven-
tion are difficult to interpret because most have
used these in combination with other strategies
such as hydrolysed formulas (26, 27), maternal
restrictions (28) and/or other environmental
interventions (26, 28). Furthermore, dietary
interventions also varied widely between studies
(restricting ÔanyÕ complementary feeding for
between 3 and 6 months and restricting specific
solids such as egg, dairy, wheat, nuts, fish and
soy up from between 4–12 months). Although
some of these studies reported benefits on some
allergic outcomes, the findings are not consistent
and difficult to attribute specifically to infant
dietary restrictions. Finally, in countries where
early dietary restrictions (of complementary
foods) have been adopted into practice such as
378
the USA (3), the UK (4) and Australia (5), rates
of food allergy have escalated rather than
declined.
New studies aimed at using early food allergen
exposure to prevent allergy
Challenging many long-held concepts, there are
now studies (in progress and in design) that will
examine the hypothesis that earlier introduction
(rather than avoidance) and regular exposure to
ÔallergenicÕ foods (such as peanuts and egg) may
reduce the risk of specific allergies to these
foods.
There is currently a UK-based randomized
controlled trial investigating the regular con-
sumption vs. avoidance of peanut protein during
infancy. This trial involves infants (4–11 months
of age) with egg allergy, severe eczema or both.
The intervention group is fed at least 6 g peanut
protein weekly, distributed over at least three
meals each week. The primary outcome of this
study assesses the effects of this intervention on
the proportion of children with peanut allergy at
5 yr of age. There is also a proposed Australian
study that will examine the effects of early egg
introduction in high-risk infants.
Other implications: growth, development and nutritional
status
The age when constituent breast milk consump-
tion will no longer meet infant nutrition require-
ments is ill-defined. Current nutrient reference
values (NRV) and energy requirements for the
first 6 months are largely based on average
intakes of healthy breastfed infants. Despite the
rapid growth and development of infants during
this period, many references ranges do not
increase until 7 months when solid foods are
currently recommended. Thus, NRV tend to be
based more in feeding practice rather than
physiological needs. A systematic review by
Lanigan et al. (29) showed a paucity of random-
ized trials and little evidence to support a change
in recommended commencement of solids to
6 months.
There are concerns that delayed introduction
of complementary feeding could compromise
supply of nutrients essential for growth and
neuro-development. Exclusive breastfeeding for
6 months has been associated with a higher risk
of anaemia (10%) compared with breastfed
infants receiving complementary feeding (2.3%)
(30). The WHO systematic review (31) also
reported that infants exclusively breastfed to
6 months had a lower haemoglobin (p = 0.005)
 Early complementary feeding in the development of oral tolerance
and ferritin level (p = 0.04) compared with
those infants fed mixed breastfeeding at
4–6 months. Delayed complementary feeding
may in some populations increase the risk of
deficiencies of iodine (32), zinc (33) and other
specific micronutrients (34). This raises particu-
lar concerns that some infants may become
deficient in essential micronutrients if solid foods
are delayed. In addition to implications for
growth, there are numerous other developmental
issues surrounding the timing of dietary diver-
sity, including the development of taste and food
preferences, which also need to be addressed in
this process.
Conclusions
New studies that address the role of early
exposure to allergenic foods (rather than avoid-
ance) are greatly needed and awaited with utmost
interest. However, until these studies have been
completed, this issue is likely to remain unre-
solved. In the meantime, there is conflict between
some allergy prevention guidelines that recom-
mend introductions of complementary foods
from Ô4 to 6 monthsÕ [e.g. as currently recom-
mend in Australia (11)] and the recommendation
for exclusive breastfeeding until Ô6 monthsÕ [by
the WHO and many other international govern-
ment and professional bodies]. The evidence for
delayed introduction of complementary foods to
6 months is very limited and difficult to justify in
the face of emerging evidence that this may be
detrimental. Rather, there is a growing case for
further revising the recommended age for the
introduction of complementary foods to
Ô4 monthsÕ while breastfeeding is maintained for
at least 6 months where possible.
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