Eczema, asthma and allergy
Jean Gelding”, Pauline M. Emmett, Imogen S. Rogers
Unit of Paediatric and Perinatal Epidemiology, Institute of Child Health, University of Bristol,
24 Tyrtdall Avenw, Brisrnt BSS ITQ, UK
Abstract
The literature in relation to the development of atopic and allergic disorders has been
reviewed, in order to assess the claim that prolonged and exclusive breast feeding protects
against the development of such disorders. The data in the literature show little consistent
evidence to identify any protective association between breast feeding and either eczema,
wheezing/asthma or other types of atopy or allergic response. 0 1997 Elsevier Science
Ireland Ltd.
Keywords: Breast feeding; Eczema; Asthma; Wheezing; Allergy; Atopy
1. Introduction
Received wisdom states that breast feeding protects a child from allergy. Advice to
mothers, particularly if there is a family history of asthma, eczema or hay fever, has
been that exclusive breast feeding is vital to protect the child from developing allergic
or atopic responses. In this paper we examine the evidence for this point of view.
There are three types of studies addressing this question-(i)
studies of whole
populations of children, regardless of family history; (ii) studies confined to children
with a family history of asthma or eczema; (iii) studies confined to children with a
specific disorder. Each published study based on reliable numbers will be discussed in
some detail.
2. Population
studies
The first population study was reported in 1936 [I]: follow-up of 20 061 infants to
nine months
of age reported
dramatic
differences
in prevalence
*Corresponding author.
0 1997
037%3782/97/$17.00
PII SO378-3782(97)0005%3
Elsevier Science Ireland Ltd.
All rights
reserved
of eczema
with
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J. Gold@
et al. I Early Human Development 49 Sup@ (1997) SIZl-S130
feeding habit. In comparison with totally breast fed infants, those partially breast fed
had twice the prevalence, and those never breast fed, seven times the prevalence.
These differences were highly significant. No subsequentpopulation study has been
able to reproduce such dramatic findings however, and the findings may be
consequent upon the artificial feed preparation used (boiled cows’ milk with cane
sugar).
The Christchurch Child Development Study is a prospective study in New Zealand
following a cohort from birth. Important analyses have assessedcomponents of the
diet during the first four months of the child’s life and its relationship with early
childhood eczema [2]. The authors found that the rate of eczemaincreasedin almost
direct proportion to the number of different types of solid food that the child had been
given during the first four months, but that breast feeding itself had no significant
relationship with eczema rates. The 1110 children were studied further and the
analysis showed no association between the rates of asthma and either breast feeding
or the introduction of weaning foods [3]. This was regardlessof whether or not there
was a parental history of asthma.
A study from Tuscan, Arizona carefully followed up 1246 healthy infants born
between 1980 and 1984 [4]. Detailed assessmentsof the health of the children were
made at defined intervals by paediatricians. Feeding patterns were identified at
well-baby clinic visits and from questionnairescompleted by the parents. By the end
of the first year of life, 33% of children had had a lower respiratory tract illness and
20% of children had had wheezing attacks. The study showed that among children
breast fed for less than one month or not at all, 12.3% had started wheezing by four
months of age; the prevalence for children breast fed for one to three months was
8.1% and for four + months was 5.2% (P < 0.005). Logistic regression in this study
allowed for maternal education, maternal smoking, ethnic origin, child’s sex, whether
either parent reported childhood respiratory problems themselves, whether others
slept in the same room as the child and the type of day care. When all confounding
variables were entered into the model, bottle feeding was still significantly associated
with early wheezing illnesses [odds-ratio (OR) 1.71but with much reduced significance (PCO.05).
A national sample of 5672 children in the United States concentrated on the
analysis of factors relating to the development of asthmaor wheeze [5]. In this study,
asthma was defined as diagnosed by the local doctor. Analysis of the data using
logistic regression allowing for birthweight, maternal age, gestation, the child’s body
mass index, triceps skinfold thickness, energy intake as well as socio-economic
factors such as low income and living in the centre of a city, resulted in a
non-significant association between breast feeding and asthma. Those bottle fed had
an OR for asthmaof 1.1 (95% CI, 0.78-1.56) and for wheeze (i.e. wheezein the past
twelve months apart from colds or ‘flu) an OR of 1.31 (95% CI, 1.01-1.70) P < 0.05.
It should be noted here, however, that parental smoking was not considered,and may
well have confounded the result.
A study of allergic diseasesin children was mounted in Sweden on the basis of a
questionnaire sent to 20 000 parents of school children aged seven, ten and fourteen
J. Gold&
et al. I Early Human Development 49 Suppl (1997) SIZI-5’1.30
s123
years of age [6]. The authors documented asthma prevalence as 2.4%, eczema at
7.8%, and total allergic diseasesincluding hay fever at 16.9%. There was considerable geographic variation throughout the country and, as expected, a parental history
of allergy was associated with a two to nine times increased incidence in the
offspring. Children, both of whose parents had a history of allergy, were shown to
suffer a cumulative effect. The authors showed from the data available that although
breast feeding appearedto postpone allergic disease,this was only true of children
with both parents having a history of allergy (P < 0.01). It should be noted, however,
that multivariate analyses were not undertaken in this study.
A study of the effects of breast feeding was carried out in the Isle of Wight in the
UK [7]. By one year of age, it was shown that those children one or both of whose
parents had a history of atopic disease were more likely themselves to exhibit
manifestations of allergy, than infants from non-allergic families. The authors
reported that breast feeding apparently gave some protection against respiratory tract
allergies, but eczemawas found as often in the initially breast fed as in the initially
bottle fed. On follow-up of thesechildren to their fourth birthday, the authors showed
that breast feeding was still not associatedwith eczema,whether or not one included
those known to have been exclusively breast fed as opposed to those who also
received supplementary milk. In fact more eczema was reported in the breast fed
group. At four years, the initial apparent association with asthma found at one year
had vanished and the breast fed group of children were as likely to have developed
asthmaas the non-breastfed group. The authors explained the difference between the
one and four year results by the inclusion of many casesof bronchiolitis in the first
year.
There have been several studies from the 1970 birth cohort which followed-up
14 000 infants born in one week throughout Great Britain. An analysis was made of
the children who by the age of ten were reported to have wheezed after twelve
months of age [S]. Seventeenpercent of children had had such a history. Logistic
regression, taking account of maternal smoking, paternal smoking, paternal absence.
sex of the child, family allergy symptoms, crowding in the household, dampnessof
the bedroom, gas cooking and heating and social status, showed an OR for not being
breast fed of 1.22 (95% CI, 0.97-1.53), which was not statistically significant.
Analyses from this study concerning childhood eczema considered the development of this disorder by the age of five. Unadjusted associations showed a positive
relationship between duration of breast feeding and onset of eczemain the first five
years [9], but logistic regression analyses resulted in this association disappearing
[lo]. The authors concluded “There is very little evidence to suggestan association
between breast feeding and eczema as reported by the mother. and certainly no
evidence of any protective effect of breast feeding. Furthermore the possibility of
such a relationship pertaining solely to infants of mothers with a positive history of
atopic disorders can be discounted:... the first order interactions between breast
feeding and the two atopic history variables were both non-significant”.
Population studies have also assessedrelationships with allergy using skin prick
criteria. Such a study was undertaken of 930 children aged between nine and fifteen
S124
J. Gelding et al. I Early Human Development 49 Suppl (1997) S121-S130
years in six Italian towns [ 111.They were skin prick tested and defined as atopic if at
least one skin prick test caused a weal greater than 3 mm diameter. Their family
history of allergy, personal allergy, medical history, allergic symptoms, exposure to
allergens, infant feeding and parents’ occupations were recorded and logistic multiple
regression analysescarried out. The significant findings concernedthe area in which
they lived, housing conditions, exposure to environmental allergens, history of
rhinitis, asthmaand/or eczemaand breast feeding. However, the relationship of atopy
with breast feeding was not in the direction anticipated by the authors,-both
unadjusted and adjusted data indicated that breast feeding was positively associated
with atopy.
A study in a totally different environment in eastern Nepal of children aged
between five and fifteen also tested for allergy using the skin prick method [12]. The
authors identified one in five children as being skin prick positive to at least one of
the allergens, and one in five as having symptomsof allergic disease,but pointed out
that there was no relationship between the symptomsand the skin prick positive tests.
They found no relationship whatsoever between the skin prick test results and the
length of time the child was breast fed. It should be pointed out that this was an area
in which breast feeding was initiated in all except three of the 293 children involved,
nevertheless,more than half these children had ceasedto be breast fed by the fourth
month of age.
A study from Denmark identified 39 children from 1749 that were being followed
prospectively from birth as fulfilling criteria for the development of cows’ milk
allergy [ 131.Seventeenof them had developed the symptoms during breast feeding,
before the age of three months. By our calculations from their published data this
implies that 1 in 100 children receiving breast milk apparently exclusively are likely
to develop cows’ milk allergy. The authors found, however, that all 39 children had
been given formula in the newborn nursery. Only 210 of the 1749 infants were not
given such supplements-none developed cows’ milk allergy (but this was not
statistically significant).
A Canadian study followed 787 babies until the secondyear of life and undertook
detailed challenge studies to identify cases of cows’ milk allergy. This occurred
among 26 (7.0%) of 374 breast fed and 33 (8.0%) of 413 bottle fed children-a
non-significant result. The authors concluded: “There is no evidence from this data
that babies brought up on the breast for a few months are protected from cows’ milk
allergy” [14].
In Finland [15] the effect of exclusive breast feeding through the first birch pollen
seasonwas examined in 59 children and compared with 67 children on cows’ milk
formula and 27 children who started breast feeding but were weaned onto formula
during the first birch pollen season.The authors showed that exclusive breast feeding
throughout the first birch pollen season did not prevent birch pollen allergy and
indeed feeding cows’ milk-based formula during this seasonseemedto protect from
subsequentdevelopment of such an allergy. Similar results were obtained in regard to
allergy to grass pollen. The authors suggestthat immunological stresson the young
infant provided by the introduction to cows’ milk at an early age may have had this
unexpected benefit.
1. Gelding et al. ! Early Human Development 49 Suppl (1997) SIZI-S130
3. Studies of children
fit25
with a family history
A number of studies of children with a family history have been undertaken. One
in London enrolled 73 infants with a parent who had a history of hay fever or asthma
[ 161.The parents kept a diary of their feeding methods and smoking habits, and the
date of the first cows’ milk feed was recorded. The children were clinically examined
at birth, at three, six and twelve months, and annually thereafter. Almost half (36) of
the children developed eczemaand 32 developed one or more episodesof wheezing,
Fifty-five percent of the children had received exclusive breast milk during the first
four weeks of life, but only 12% were totally breast fed for the first three months.
There was no evidence from this study that breast feeding was protective-whether
one measuredatopy by a positive skin test, the presenceof eczemaor a combination
of the two. Indeed, the highest rate of the latter category (skin test positive and
eczemapresent) was in children who were breast fed for longer than thirteen weeks
(five (55%) out of nine), comparedwith 16 (25%) of 64 children who were breast fed
for less than this. The strongest relationship with wheeze was parental smoking.
Businco et al. [17] had followed 101 babies with a familial history of asthma,hay
fever or eczemauntil the age of two. If the mother was successfully breast feeding by
two weeks, she was encouraged to restrict her own intake of cows’ milk to 200
ml/day and to have no more than two eggs/week. If she needed/wanted to
supplement or give up altogether, the baby was given a soy basedformula. Weaning
foods were not given until six months and then restricted to those thought not to be
allergenic until nine months. The comparison group had either never breastfed, or not
done so for longer than two weeks. The babies were given cows’ milk formula, and
no restriction was placed on weaning food. This study resulted in the statementthat
breast feeding + soy supplements“exerts a prophylactic effect on the development of
atopic disease”. This widely quoted study did no statistical tests-and indeed had
they done so they would have had to report no significant effect [ 1S].
A study from Northwick Park Hospital [19] followed 92 children who had at least
one atopic parent, to the age of five years. Skin prick tests and immunoglobulin E
(IgE) antibody levels were measured over time. The authors stated that “Breast
feeding was associatedwith an increase in the prevalence of positive results in skin
tests,but was not associatedwith detectableIgE antibodies to food proteins... and was
not associatedwith protection against the development of disease”.
Kaufman and Frick [20] followed 94 infants of allergic mothers to the age of two:
38 were breast fed-two (6%) of these developed asthma, whereasten ( 18%) of the
56 bottle fed infants did so (p < 0.06). Although the authors did not report the
prevalence of eczemain breast as opposed to bottle feeding, they noted that among
those who had eczema,those who were bottle fed were significantly more likely to
develop asthmathan those who were breast fed-but the numbers involved were not
given-and consequently are impossible to interpret.
In Canada, 37 children who had an older sibling with allergic disease and were
exclusively breast fed for the first six weeks of life or longer, were compared by
Chandra with 37 who had a similar older sibling but were fed cows’ milk formula
[21]. There were statistically significantly lower rates of eczema V’< 0.001).
S126
J. Golding et al. I Early Human Development 49 Suppl (1997) S121-S130
recurrent wheezing (P<O.Ol), high serum IgE (P <O.OOl), and other biochemical
markers indicating a reduced risk of allergy in the breast fed as opposed to the
formula fed children.
A further study by Chandra and colleagues was a randomised controlled trial of
three different formulae-a whey hydrolysate formula, a conventional cows’ milk
formula and a soy based formula; these three groups were also compared with a
group of mothers who breast fed exclusively for four months or longer. There were
72 children in each of the four groups. It is not clear to what extent the breast fed
group was similar to that of the three randomised groups, but the authors concluded
that “Exclusive breast feeding for more than four months is partially protective
against the development of atopic disease among high risk infants. Among those not
breast fed, feeding a milk/whey hydrolysate formula to infants at high risk because of
history of atopy among first degree relatives reduces the incidence of atopic disease
and this approach is significantly beneficial compared with breast feeding without
maternal dietary restriction or feeding a soy based formula” [22].
The largest and most notable study was of 519 infants in South Wales whose
mothers were participating in a randomised controlled trial of withholding cows’
milk, and substituting soya milk for those who were not breast fed; infants were
followed up and examined for evidence of allergic disease at three, six and twelve
months of age. Analysis of the factors in these children that predicted wheeze, treated
the study as though it was an observational survey [23]. Logistic regression allowed
for the number of siblings, the season of birth, the sex of the child, whether damp was
present in the home, mother’s smoking habit and social class of the household. In the
presence of these factors, the authors identified a statistically significant decrease in
wheezing in children who had ever been breast fed (OR 0.53, 95% CI, 0.33-0.86,
P < 0.01). There was no significant difference, however, in the prevalence of eczema
between those who had been breast fed at all and those who had never been breast
fed. Subsequent follow up to age seven of 453 of these children [24] showed that
although the reduced rate of wheezing persisted in children who had received breast
milk, this was only found in children who were not atopic. Burr and colleagues
showed that wheezing with onset in the first two years was much more likely to have
an infectious aetiology than wheezing with later onset. They concluded that breast
feeding protects against wheezing episodes initiated by infection but not against
asthma.
4. Studies confined to children
with specific histories
A study from Iraq [25] considered 100 children with wheezy bronchitis and
showed that more of this group were breast fed when compared with children of
similar ages who were attending a vaccination clinic. The authors suggested that the
mechanism involved rapid growth of the breast fed infants in this community, since
the immune properties of breast milk are likely to have given protection from severe
infection and resultant malnutrition. In Iraq supplementing breast milk with cheap
.I. Golding et al. I Early Human Development 49 Suppl (1997) S121-S130
S12?
starch products such as biscuits is a common practice, resulting in overweight
children who are commonly seen with wheezy bronchitis.
Investigators in Israel followed prospectively the clinical course of diseasein 80
atopic wheezing babies from six months to five years [26]. They statedthat there was
no correlation between changesin IgE levels and early feeding with breast or bottle
milk, but that persistent wheezing in these children was associatedwith both bottle
feeding and parental smoking. Their statistical analysis did not adequatelydistinguish
whether one of these factors explained the other.
An Australian study which had identified 371 seven year old children with
wheezing and followed them up until 21 years of age, categorised the types of
wheezing and asthma into four grades [27]. The authors found that those subjects
with the most severewheezing at age 21 were more likely to have been breast fed in
infancy and for longer periods than the group with no symptomsor those with mild or
moderateasthma.The authors suggestthat “further investigation is neededbefore the
hypothesis that breast feeding protects against the development of allergic phenomena
can be accepted”.
In one study 49 children with eczema who were exclusively breast fed and had
never received anything except breast milk were compared with 34 similarly fed
infants but without eczema[28]. Almost half the children with eczemawere shown to
be hypersensitive to foods such as egg and cows’ milk (23 out of 49). Breast milk
samples were collected from nineteen mothers after the ingestion of egg, but
ovalbumin was detectedin similar concentrationswhether the mother had a child with
eczema or not.
A study from Canada[29] investigated nineteen children with IgE mediated allergy
associatedwith positive skin prick tests to peanut, cows’ milk and/or egg. In all.
seventeenof the children had been breast fed, ten exclusively for at least five months.
Since reaction to the foods had occurred on first exposure to the food in almost all
instances, it was proposedthat sensitisation had occurred antenatally or via the breast
milk. A study of the mothers of sensitisedchildren showed that they did not consume
more of these foods than the mothers of non-sensitised children and indeed,
avoidance of the foods by some mothers did not ensure freedom from sensitisation.
They concluded “Breast feeding by itself cannot be guaranteedto protect against the
development of food allergy”.
5. Discussion
Chandra [30] suggestedthat there are “at least five possible reasonsfor expecting
breast fed infants to show a reduced occurrence of atopic disease.Firstly, breast fed
infants are less exposed to ‘foreign’ dietary antigens. Secondly, human milk is
postulated to contain factors that mature the intestinal mucosa,thereby allowing early
‘closure’ of macromolecular absorption. Thirdly, by reducing the incidence of
infection and altering the gut microflora that can act as an adjuvant for ingested food
proteins, the possibility of sensitisation may be decreased.Fourthly, human milk has
anti-inflammatory properties that will also decreasemacromolecular uptake. Finally,
S128
J. Gelding et al. I Early Human Development 49 Suppl (1997) S121-S130
the presence of various cytokines in human milk may play an important role in
modulating the development of allergic diseases”.
How clear is it though that there is a reduction in atopic disorders? Reviews of the
literature on breast feeding and the development of allergy in the past tended to infer
that breast feeding did indeed prevent atopic or allergic disorder, but probably only
among children of affected parents [31-331.
The data from general population studies certainly lack a clear pattern. Although
the earliest study showed a protective effect for breast feeding in relation to
development of eczema in the first nine months [ 11, other studies [2,7,10] showed no
sign of any protective relationship. For asthma and/or wheezing, no protective effect
was found in one study [3], it was evident in others [4,5,7,8] although in one of these
the effect was found up to one year but not thereafter [7], and in another [8] statistical
significance was not achieved.
More general assessment of allergy using a combination of asthma, eczema, and/or
hay fever [6] concluded that although there was an initial protective effect of breast
feeding, this was only found where both parents had a history of allergy, and even in
this group, the reduced prevalence was only a postponement of development of the
disorder.
Indeed skin prick testing showed, in one population, that allergic response was
significantly more likely in children who had been breast fed [ll]. A distinction
between ever and never breast fed was unable to be made in the Nepal study as
almost all (99%) children had received some breast milk. Nevertheless, prolonged
duration did not show a benefit in comparison with short duration [12].
Among the five studies of children with a familial history, one showed no
relationship with eczema, wheezing or positive skin test [16], one showed increased
IgE antibodies among those who had been breast fed [19], one showed no
relationship with eczema but a significant reduction in wheezing in the first year of
life [23]; only the two studies by Chandra and colleagues, however, claimed
substantial benefits for breast feeding [21,22] but it is not clear how comparable the
groups were in his studies.
Some of the confusion in the studies may be due to confusion of diagnoses. This
was amply shown by the seminal study of Burr and colleagues [23,24]. Although
breast feeding was significantly associated with a reduced prevalence of wheezingthis seems to have been entirely due to a reduced prevalence of lower respiratory
infection not of asthma.
Another possible explanation for the striking difference between the protective
findings in the study of the 1930s may lie in either the fact that prolonged
unsupplemented breast feeding was common at the time, or that mothers had a more
restricted diet and were less likely to expose their infants to allergens via the breast
milk.
Criticisms of studies that fail to find a protective effect have tended to suggest
either the failure of a mother to continue to breast feed for long enough, or to have
introduced non-milk supplements too early or have failed to avoid, while breast
feeding, all those substances that might provoke an allergenic response in her child.
Reality, however, is that mothers are unlikely to conform to such restrictions without
J. Golding et al. I Early Human Development 49 Suppl (1997) Sl21-St30
s129
themselvesundergoing immense stressand anxiety. From the information available it
is the authors’ opinion that breast milk itself is likely to have such major benefits in
preventing infection that no further justification is needed for breast feeding. The
stressto a mother of restricting her own and her child’s diet in the hope of preventing
allergy (with consequentguilt if the child develops asthmaor eczema)is not justified
on the evidence available.
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