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Treatment and prevention of food allergies in breastfed infants: practice and evidence.

(Nutr Diet 2004;61:76-81)

Abstract

Objective: To determine whether current Australian dietetic practice is consistent with research relating to maternal dietary restrictions for treatment and prevention of food allergy in breastfed infants.

Design: Mail survey to benchmark practice and a systematic review of relevant studies and trials.

Subjects and setting: All 15 Australian specialist paediatric allergy dietitians were surveyed. The systematic review was confined to studies involving maternal dietary intervention followed by maternal dietary challenge for the treatment of breastfed infants with food allergy, trials investigating maternal dietary restriction during lactation for allergy prevention, and studies where food proteins have been detected in human milk after the ingestion of a specific food challenge.

Main outcome measure: Assessment of current practice in relation to the level and quality of evidence on food allergy treatment and prevention in breastfed infants.

Results: The majority of dietitians (13 out of 15) surveyed follow recommendations of expert committees that breastfed infants with food allergy symptoms are trialled on maternal dietary restriction. However, the strength of published evidence in this area is limited and high quality randomised controlled trials are required to test the validity of current practice and recommendations. Maternal dietary restrictions to prevent food allergy were used by six of the 15 dietitians surveyed. No clinical trials have investigated maternal dietary restriction during breastfeeding with the specific outcome of reducing the development of food allergy.

Conclusion: Insufficient high quality evidence exists to determine the extent of benefit offered by maternal food avoidance diets to breastfed infants for the treatment and prevention of food allergy.

Key words: food allergy, human milk, food proteins, maternal diet, practice survey

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Introduction

Food allergy diagnosis requires the determination of a causal relationship between the improvement of symptoms after commencing a strict avoidance diet for a suspected food protein followed by the return of these symptoms on food challenge (1). The incidence of food allergy in exclusively breastfed infants, with symptoms of eczema, colic, diarrhoea and vomiting, is approximately 0.5% (2,3). For the treatment of these breastfed infants there is a consensus from both European and American expert committees that a trial of maternal dietary restriction should be undertaken (1,4).

Strategies to prevent food allergy in infants who are at high risk because of a strong atopic family history are controversial. Most recommendations include exclusive breastfeeding or use of a formula with confirmed reduced allergenicity for at least four to six months and not introducing solid foods before five to six months of age (1,4,5). The use of maternal dietary restriction during lactation to treat food allergy in breastfed infants led to the hypothesis that maternal dietary restriction during lactation may also prevent the development of food allergy in breastfed infants. The American Academy of Pediatrics, Committee on Nutrition (4) has recommended that mothers of high risk infants should eliminate peanuts and tree nuts, and also consider eliminating eggs, cow's milk and fish from their diets while breastfeeding. However some regard this approach as experimental (5).

In this paper we review current Australian dietetic practice and systematically examine the research regarding the use of maternal dietary restrictions to treat and prevent food allergy in breastfed infants.

Methods

Survey of current dietetic practice in Australia

A survey was mailed to all major paediatric hospitals in Australia and other known specialist paediatric allergy dietitians at ACT Community Care. Flinders Medical Centre, John Hunter Hospital, Mater Health Services Brisbane, Monash Medical Centre, Princess Margaret Hospital, Royal Children's Hospital Brisbane, Royal Children's Hospital Melbourne, Royal Hobart Hospital, Royal Prince Alfred Hospital, Sydney Children's Hospital. The Children's Hospital at Westmead, The Murdoch Institute, plus two dietitians in private practice specialising in allergy. A total of 15 specialist dietitians were identified. This survey was constructed to determine the extent of maternal dietary restrictions advised by dietitians to breastfeeding mothers to treat or prevent food allergy in their infants. Where dietary restriction was used, questions were asked regarding circumstances, the extent of foods avoided and whether partial or complete avoidance of these foods was recommended. Where dietary restriction was not used, the reasons for this practice were also ascertained. The survey was approved by the Research Ethics Committee of the Women's and Children's Hospital. A copy of the survey can be obtained on request from the corresponding author.

Literature review of evidence

The medline database was searched using terms: food protein (+cow's milk, nut, egg) and breast (human) milk; food allergy treatment; food allergy prevention; maternal food challenge; food allergy and breastfed infants. The search was limited to human subjects and English language articles. The data of the last search was 19 March 2003. Research evidence retrieved and considered for this review included: studies involving maternal dietary restriction followed by maternal dietary challenge to treat breastfed infants with food allergy; trials investigating the use of maternal dietary intervention during lactation to prevent allergy in high-risk breastfed infants; studies where food proteins have been detected in human milk after the ingestion of a specific challenge dose of food. NHMRC levels of evidence criteria were used to assess the quality of the study design (6).

Results and discussion

Survey of current dietetic practice in Australia: treatment of food allergy

All 15 major paediatric hospitals and other known specialist paediatric allergy dietitians surveyed responded. The majority of dietitians (13 out of 15) surveyed follow the recommendations of expert committees that breastfed infants with food allergy symptoms be trialled on maternal dietary restriction (1,4). There is also agreement that the foods most commonly restricted are cow's milk, egg, peanut and tree nuts. Nine out of 13 dietitians advise complete rather than partial dietary avoidance of these food proteins. Treatment was individualised, and the most common circumstances for advising dietary interventions were if the food allergy symptoms commenced when the infant was exclusively breastfed and/or the breastfed infant had severe symptoms.

Literature review of evidence: treatment of food allergy

The treatment of suspected food allergy in breastfed infants with symptoms of atopic dermatitis/eczema, colic, diarrhoea and vomiting by maternal dietary restriction, and confirmation of this diagnosis and treatment effect with maternal dietary challenge has been described (2,7-14). Although results in some of these studies appear impressive, many are case series (2,7,8,12,14) where the dietary interventions were non-randomised and uncontrolled with open food challenges (NHMRC level of evidence IV) (6).

Only three studies in the area (9-11) (Table 1) were randomised trials of crossover design with double-blind food challenges (NHMRC level of evidence II (6)). The choice of an appropriate placebo challenge for such trials should be a non-allergenic food. Unfortunately two of these trials (9,11) used potentially allergenic soy protein for placebo challenges, which may explain the lack of difference in symptoms observed between challenge foods. This leaves only one randomised controlled trial conducted in 1983 (10), where nine out of 16 infants had colic symptoms following maternal ingestion of cow's milk capsules but not after the appropriate non-allergenic placebo of potato starch capsules. The mothers participating in this trial were, however, pre-selected after an initial period of colic symptom improvement following maternal cow's milk avoidance and symptom return on open maternal cow's milk challenge. This may have biased the results towards a more positive response than if any group of infants with colic symptoms were studied.

Thus, despite widespread recommendations and practice of maternal food protein avoidance to treat food allergy in breastfed infants, the strength of published trials is limited. Research evidence of improved quality is required from large, randomised, appropriately placebo controlled, double-blinded food exclusion and challenge trials to test the validity of current practice and substantiate recommendations.

Survey of current dietetic practice in Australia: prevention of food allergy

Nine out of 15 dietitians surveyed reported that they do not advise maternal dietary restrictions for lactating women with a family history of allergy in order to prevent food allergy in their infant. The most common reason given was the lack of scientific evidence that food proteins in breast milk may adversely affect the infant. Six of 15 dietitians reported they would advise maternal dietary restrictions for food allergy prevention, especially if the infant has a sibling with food allergies. Again the advice was individualised, however all of these six dietitians would recommend that peanuts be completely avoided, in keeping with the recommendation from the American Academy of Pediatrics committee (4).

Literature review of evidence: prevention of food allergy

The use of maternal dietary restriction during lactation to prevent allergy in high-risk infants (due to an atopic family history) has been investigated in trials that are summarised in Table 2 (15-22). Three of these trials (15,16,20) were also included in the Cochrane Review on this topic (23). The main infant outcome measures in these trials were atopic disorders determined by clinical examination. Several of these trials demonstrated significant reductions in atopic dermatitis/eczema between groups following maternal and infant dietary interventions compared with control groups following unrestricted diets (15-17,19,20). To determine whether maternal dietary restriction during lactation prevents food allergy, the outcome measures should include double-blind, placebo-controlled food challenges. Skin prick testing to food allergens (17-19,22) or IgE levels specific to food allergens (21), as an indicator for food allergen sensitisation were performed in five of these trials, however food challenges to confirm the diagnosis of food allergy were only done in two studies (18,19), with only one using double-blind, placebo-controlled food challenges (18).

Although the intervention in all trials included dietary restriction in lactating women, the type and number of foods avoided and length of dietary restriction varied (Table 2). In some cases dietary intervention began in pregnancy (18,19). Some trials also applied infant dietary interventions, through the use of hydrolysed formula when breastfeeding ceased (18-20). Others compared the introduction of solids guidelines (18,19). Therefore it is not possible to determine the relative importance of maternal food avoidance during lactation compared with the other infant interventions. Interestingly only three studies (17,21,22) specifically investigated maternal dietary restriction during lactation. These studies reported no significant differences in rates of specific food sensitisation measured by IgE levels or skin prick tests, but the presence of symptomatic food allergy was not documented by means of food challenges. Thus no trials to date specifically investigated maternal dietary restriction during breastfeeding alone and confirmed the final outcome of food allergy development by means of food challenge.

Detection of food proteins in human milk

The premise that maternal dietary restrictions during breastfeeding may benefit the infant assumes that ingested food proteins are absorbed and excreted antigenically intact into breast milk. Table 3 summarises those studies where food proteins have been detected in human milk after the ingestion of a specific challenge dose of food including: ovalbumin (egg) (24,25), bovine [beta]-lactoglobulin (cow's milk) (2,12,24,26-28), gliadin (wheat) (29) and Ara h 1 and Ara h 2 (peanut) (30). Results from these studies show that even after the ingestion of the same challenge dose of a particular food the frequency and concentration of detected food protein in breast milk varies (Table 3). The factors which account for this wide variation in the detection of food proteins in human milk remain unexplained but may be critical in understanding the effect of maternal dietary restriction during lactation for the treatment and prevention of food allergy.

[beta]-lactoglobulin from cow's milk (2,12,24,26-28) has been the most commonly studied food protein. However the measurement of bovine [beta]-lactoglobulin in human milk using polyclonal antibodies by enzyme linked immunosorbent assay (ELISA) or radioimmunoassay (RIA) could lead to inaccurate results as these antibodies have been demonstrated to also detect the presence of human milk proteins such as lactoferrin, [beta]-casein and [alpha]-lactalbumin (31). In a study measuring gliadin in human milk (29) the concentration and frequency of detected gliadin decreased with increasing stage of lactation. This may relate to the decrease in total protein concentration in breast milk as lactation progresses (32). Table 3 illustrates the wide range of lactation stages in previous studies, which may account further for some of the variability in results observed. Repeat measures of the same ingested challenge dose on different days on the same woman would be necessary to determine intra-individual variation on the presence of food proteins in human milk. Previous studies have not addressed this issue.

Studies investigating a dose-related effect of food protein ingested on breast milk concentration have not yet been published. Thus current available evidence is lacking on the required extent of dietary avoidance of food proteins in the maternal diet. In agreement with an expert European committee (1), most of the Australian dietitians surveyed (nine out of 13) advise complete avoidance of the causal protein from the diet of the lactating mother to treat food allergy in breastfed infants. However, we should not forget that total dietary avoidance of one or more food proteins is difficult to achieve, can be nutritionally compromising, time consuming and socially restrictive for breastfeeding mothers. If complete maternal dietary avoidance is recommended for treatment, what about prevention? Kilburn (22) has proposed that exposure to low-dose food allergens via breast milk may produce tolerance rather than sensitisation. Breast milk contains immune components, such as IgA antibodies, which are thought to bind to food proteins to form immune complexes decreasing the chances of these food proteins from crossing the intestinal surface in a breastfed infant. Jarvinen (33) demonstrated that total IgA levels in breast milk were significantly lower in mothers who had infants with cow's milk allergy compared to those without cow's milk allergy, suggesting that low maternal IgA levels in breast milk may be an important factor in infant allergy development. It is also possible that infants may be sensitised in utero, either directly or by transplacental passage of allergen, however the Cochrane Review (23) on maternal dietary antigen avoidance during pregnancy concluded that prescription of an antigen avoidance diet to a highrisk woman during pregnancy is unlikely to substantially reduce her child's risk of atopic diseases, and such a diet may adversely affect maternal and/or foetal nutrition. Other possible routes of sensitisation for breastfed infants to food proteins may include contaminated hands (1), inhaled food proteins (1) or contact with inflamed skin (34).

Conclusion

Although on the surface it would appear to be a logical precaution for breastfed infants, evidence on the use of maternal dietary restriction to treat food allergy is of limited strength, and evidence on the use of maternal dietary intervention to specifically prevent food allergy has not been addressed. Furthermore, the current scientific literature does not address questions about the extent and duration of dietary food avoidance. It is also important to understand which factors may influence the presence of food proteins in human milk. This knowledge will aid the design of large, randomised, appropriately controlled, blinded trials to investigate the use of maternal diet restriction during lactation for both the treatment and prevention of food allergy in breastfed infants.
Table 1. Trials on maternal dietary restriction and challenge in
treatment of breastfed infants with food allergies

 Study design, sample
 size and level of Maternal dietary
Study evidence (a) restrictions

Jakobsson Randomised, crossover cow's milk
1983 (10) design with double-
 blind challenge,
 followed by an open
 challenge (n = 16) II (a)
Evans Randomised, crossover cow's milk
1981 (9) design with double-
 blind challenge (n = 20)
 II (a)
Cant Randomised, crossover cow's milk, egg, chocolate, nuts,
1986 (11) design with double- wheat, fish, beef, chicken, citrus
 blind challenge (n = 19) fruits, colourings & preservatives
 II (a)

 Maternal dietary
Study challenge Results of maternal diet challenges

Jakobsson cow's milk vs potato 9 out of 16 infants with infantile
1983 (10) starch capsules, colic symptoms after cow's milk
 followed by open capsules and cow's milk drink, but not
 challenge of 1/2 to 1 after placebo potato starch capsules.
 glass cow's milk 3
 times per day
Evans 600 ml flavoured soy Maternal cow's milk avoidance resulted
1981 (9) milk vs flavoured in no reduction in infantile colic.
 300ml soy + 300 ml
 cow's milk drink
Cant soy milk powder vs Mean values of atopic eczema scores
1986 (11) cow's milk and egg not significantly different between
 powder (600 ml milk soy vs cow's milk and egg challenges.
 and 1 egg per day)

(a) NHMRC levels of evidence (6).

Table 2. Trials on allergy prevention in breastfed infants with maternal
dietary restriction

Study Study design Sample size

Chandra Randomised trial with 121 enrolled
1986 (15) non-blinded examination 12 withdrew, D = 55 and
 II (a) ND = 54 completed
Chandra Randomised trial with 112 enrolled
1989 (16) blinded examination II (a) 15 withdrew, D = 49 and
 ND = 48 completed
Hattevig Cluster trial of two towns 115 enrolled
1989 (17) with non-blinded 6 withdrew, D = 65 and
 examination III-1 (a) ND = 50 completed
Zeiger Randomised trial with 379 enrolled
1989 (18) blinded examination II (a) 91 withdrew, D = 103 and
 ND = 185 completed
Arshad Randomised trial with 136 enrolled
1992 (19) blinded examination II (a) 16 withdrew, D= 58 and
 ND = 62 completed
Lovegrove Randomised trial with 44 enrolled
1994 (20) blinded examination II (a) 6 withdrew, D = 12 and
 ND = 14 completed (12 non-
 atopic women)
Herrmann Participants self-selected 150 enrolled
1996 (21) their intervention group 12 withdrew, A = 30, B = 33
 with non-blinded and C = 41 completed
 examination III-2 (a) (34 mothers breastfed < 3
 months)
Kilburn Participants self-selected 111 enrolled
1998 (22) intervention group with 4 withdrew, D = 13 and
 blinded examination ND = 94 completed
 III-2 (a)

Study Maternal diet & infant interventions

Chandra D = cow's milk, egg, beef, fish, peanut-free diet for
1986 (15) mothers throughout pregnancy and lactation
 ND = no diet restrictions for mothers
Chandra D = cow's milk, egg, fish, peanuts, soybean-free diet for
1989 (16) mothers for first 6 months of lactation
 ND = no diet restrictions for mothers
Hattevig D = cow's milk, fish, egg-free diet for mothers for first
1989 (17) 3 months of lactation
 ND = no diet restrictions for mothers
Zeiger D = cow's milk, egg, peanut-free diet for mothers for
1989 (18) last trimester of pregnancy and during lactation (d) +
 solid restrictions for infants
 ND = no diet restrictions for mothers or infants
Arshad D = cow's milk, fish, nut, egg-free diet for mothers for
1992 (19) first 9 months of lactation (d) + solid restrictions for
 infants and anti-house dust-mite measures
 ND = no diet restrictions for mothers or infants
Lovegrove D = cow's milk-free diet for mothers during lactation (d)
1994 (20) ND = no diet restrictions for mothers
Herrmann A = cow's milk, egg-free diet for mothers for last
1996 (21) trimester of pregnancy and during lactation (allowed
 goat and sheep milk)
 B = cow's milk, egg-free diet for mothers for lactation
 only (allowed goat and sheep milk)
 C = mothers consumed at least 1000 ml cow's milk and
 1 egg daily
Kilburn D = cow's milk, egg, fish, nut-free diet for mothers
1998 (22) during lactation
 ND = no diet restrictions for mothers

Study Infant outcome measure Main results

Chandra Atopic eczema up to 12 months. Atopic eczema up to 12
1986 (15) months, D = 31% < ND = 44%.
Chandra Atopic eczema up to 18 months. Atopic eczema up to 18
1989 (16) months, D = 22% < ND = 44%.
Hattevig Atopic disorders at birth, 3, 6, Atopic dermatitis at 3
1989 (17) 9, 12 & 18 months. SPT (b) at 9 months, D = 3% < ND = 22% &
 months to egg, cow's milk and at 6 months,
 fish. D = 11% < ND = 28%.
 NS (c) for prevalence of
 atopic dermatitis at 9, 12
 & 18 months.
Zeiger Atopic disorders at 4, 12 & 24 Atopic disorders at 12
1989 (18) months. SPT at 4, 12 & 24 months months, D = 16% < ND = 27%.
 to food and inhalant allergens. NS for prevalence of atopic
 disorders at 4 & 24 months.
Arshad Atopic disorders at 3, 6 & 12 Atopic disorders at 3
1992 (19) months. months, D = 5% < ND = 18%,
 SPT to foods & environmental at 6 months,
 allergens. D = 12% < ND = 32% & at 12
 months, D = 14% < ND = 40%.
Lovegrove Atopic eczema at 6, 12 & 18 Atopic eczema at 18 months,
1994 (20) months. D = 11% < ND = 50%.
 NS for prevalence of atopic
 eczema at 6 & 12 months.
Herrmann Atopic dermatitis at 1, 3, 6 & NS for prevalence of atopic
1996 (21) 12 months. dermatitis at 6 & 12
 IgE specific to cow's milk & months.
 egg at 6 and 12 months.
Kilburn Atopic disorders at 3, 6, 12 & NS for incidence of atopic
1998 (22) 18 months. SPT at 6, 12 & 18 disorders at 3, 6, 12 & 18
 months to foods & inhalant months.
 allergens.

(a) NHMRC levels of evidence (6).
(b) SPT = skin prick test.
(c) NS = no significant differences.
(d) Infants had hydrolysed formula when breastfeeding ceased.

Table 3. The detection of dietary food proteins in human milk after
challenge dose ingestion

Study & Stage of Challenge Timing of
mothers lactation dose samples

Kilshaw 1 week to 12 1/2 pint cow's Prior to and at
1984 (24) months milk & 1 raw 2, 4 & 6 hours
n = 29 egg after challenge
Cant < 6 months 1 raw egg Prior to and at
1985 (25) (most 3-4 2, 4 & 6 hours
n = 19 months) after challenge
Troncone 1 week to 5 20 g gluten 2-4 hours
1987 (29) months (Prior to and at
n = 53 2, 4 & 6 hours)
(n = 6) after challenge
Cavagni not clearly 1 cooked egg 3-5 hours after
1988 (12) described & 100 g challenge
n = 13 cow's milk
Host not clearly 500 ml cow's 4 hours after
1988 (2) described milk challenge
n = 19
Host 1-2 weeks 500 ml cow's Prior to and at
1990 (26) atopic & 8-19 milk 4, 8, 12 & 24
n = 20 weeks non- hours after
 atopic mothers challenge
Sorva 2-12 months 400 ml cow's Prior to and at 1
1994 (27) (median 7 milk and 2 hours
n = 53 months) after challenge
Fukushima 4-10 months 200 ml cow's 1-3 hrs, 4-8 hrs
1997 (28) milk and 9-15 hrs
n = 24 after challenge
Vadas not clearly 50 g peanuts Prior to and at
2001 (30) described 1, 2, 3, 4, 6, 8 &
n = 23 12 hrs after
 challenge

Study & Detection Sensitivity Concentration
mothers method (ng/ml) (ng/ml)

Kilshaw RIA (a) 0.1-15 0.11-6.4 CM
1984 (24) 0.26-6.17 egg
n = 29
Cant RIA (a) 0.1-15 0.2-4.0
1985 (25)
n = 19
Troncone ELISA (b) 5 5-95
1987 (29)
n = 53
(n = 6)
Cavagni RIA (a) 0.01 results only
1988 (12) given as
n = 13 positive or
 negative
Host ELISA (b) 0.3 0.5-45
1988 (2)
n = 19
Host ELISA (b) 0.3 0.9-150
1990 (26) (median 4.2)
n = 20
Sorva ELISA (b) 0.002 0.00-8.6? (not
1994 (27) clearly stated)
n = 53
Fukushima ELISA (b) 0.1 up to 16.5
1997 (28)
n = 24
Vadas ELISA (b) Not 120-430
2001 (30) reported
n = 23

Study & Detection Peak
mothers frequency appearance

Kilshaw 52% CM 4 hours
1984 (24) 59% egg
n = 29
Cant 74% egg 2-4 hours
1985 (25)
n = 19
Troncone 68% 1 sample only
1987 (29) gliadin (at 2-4 hours)
n = 53
(n = 6)
Cavagni 62% CM (c) 1 sample only
1988 (12)
n = 13
Host 21% CM (c) 1 sample only
1988 (2)
n = 19
Host 95% CM (c) 4-24 hours
1990 (26) (median 8 hr)
n = 20
Sorva 75% CM (c) only 1 mother
1994 (27) studied > 2
n = 53 hours
Fukushima 63% CM (c) not reported
1997 (28)
n = 24
Vadas 48% 1-2 hours
2001 (30) peanut
n = 23

(a) RIA = radioimmunoassay.
(b) ELISA = enzyme linked immunosorbent assay.
(c) CM = cow's milk.


Acknowledgments

The authors would like to thank all the participating dietitians who volunteered their time to complete the survey of current practice. Part of this work was funded by grants from the Rural Industries Research and Development Corporation and the Women's and Children's Hospital Research Foundation. Maria Makrides was supported by a NHMRC RD Wright Fellowship.

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Child Health Research Institute, Women's and Children's Hospital, Adelaide and Department of Paediatrics, The University of Adelaide

D.J. Palmer, BSc, BND, APD, PhD candidate

M. Makrides, BSc, BND, PhD, Head of Applied Nutrition Group and Senior Lecturer

Department of Paediatrics, The University of Adelaide

M.S. Gold, MBCHB, MD, FRACP, Senior Lecturer

Correspondence: M. Makrides, Child Health Research Institute, Women's and Children's Hospital, 72 King William Road, North Adelaide SA 5006. Email: makridesm@mail.wch.sa.gov.au
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Title Annotation:Original Research
Author:Makrides, Maria
Publication:Nutrition & Dietetics: The Journal of the Dietitians Association of Australia
Geographic Code:8AUST
Date:Jun 1, 2004
Words:5059
Previous Article:Food allergens and food allergy--complex relationships and responsibilities.
Next Article:General nutrition-related knowledge and beliefs of post-partum women.
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