Background: Whether breast milk (BM) can protect against allergy has been studied extensively, with conflicting results. Variations in mothers’ BM composition may explain some of the conflicting results. Our aim was to assess the impact of maternal allergy and probiotic intervention on BM food antibodies, transforming growth factor (TGF)-β2 and interleukin (IL)-10 and their impact on allergy development in children until the ages of 2 and 5. Methods: We measured total IgA, IgA antibodies to cow’s milk (CM), casein, β-lactoglobulin and ovalbumin (OVA), TGF-β2 and IL-10 in 364 colostrum samples and 321 BM samples taken at 3 months from mothers participating in a prospective study evaluating the allergy-preventive effect of probiotics in a cohort with an increased risk for allergy. Results: CM, casein and OVA antibodies, TGF-β2 and IL-10 were detectable in most samples. Maternal allergy was associated with raised levels of IgA to casein (p = 0.04) and lower levels of TGF-β2 (p = 0.006) in mature BM. Probiotic supplementation was associated with increased IL-10 (p = 0.046) and decreased casein IgA antibodies (p = 0.027) in mature BM. High OVA IgA antibodies in colostrum were associated with the development of atopy by the age of 2, while low levels in mature BM were a significant risk factor for the development of eczema by the age of 2. TGF-β2 levels in BM constituted a risk for development of allergy by the age of 2. Conclusions: The immunologic composition of BM was only slightly affected by maternal atopy and could be altered by probiotic supplementation. Small effects of BM components on allergy development in children were evident.

1.
Field CJ: The immunological components of human milk and their effect on immune development in infants. J Nutr 2005;135:1–4.
2.
Kull I, Melen E, Alm J, Hallberg J, Svartengren M, van Hage M, Pershagen G, Wickman M, Bergstrom A: Breast-feeding in relation to asthma, lung function, and sensitization in young schoolchildren. J Allergy Clin Immunol 2010;125:1013–1019.
3.
van Odijk J, Kull I, Borres MP, Brandtzaeg P, Edberg U, Hanson LA, Host A, Kuitunen M, Olsen SF, Skerfving S, Sundell J, Wille S: Breastfeeding and allergic disease: a multidisciplinary review of the literature (1966–2001) on the mode of early feeding in infancy and its impact on later atopic manifestations. Allergy 2003;58:833–843.
4.
Bergmann RL, Diepgen TL, Kuss O, Bergmann KE, Kujat J, Dudenhausen JW, Wahn U: Breastfeeding duration is a risk factor for atopic eczema. Clin Exp Allergy 2002;32:205–209.
5.
Brandtzaeg P: The mucosal immune system and its integration with the mammary glands. J Pediatr 2010;156:S8–S15.
6.
Labbok MH, Clark D, Goldman AS: Breastfeeding: maintaining an irreplaceable immunological resource. Nat Rev Immunol 2004;4:565–572.
7.
Casas R, Bottcher MF, Duchen K, Bjorksten B: Detection of IgA antibodies to cat, beta-lactoglobulin, and ovalbumin allergens in human milk. J Allergy Clin Immunol 2000;105:1236–1240.
8.
Duchen K, Casas R, Fageras-Bottcher M, Yu G, Bjorksten B: Human milk polyunsaturated long-chain fatty acids and secretory immunoglobulin A antibodies and early childhood allergy. Pediatr Allergy Immunol 2000;11:29–39.
9.
Machtinger S, Moss R: Cow’s milk allergy in breast-fed infants: the role of allergen and maternal secretory IgA antibody. J Allergy Clin Immunol 1986;77:341–347.
10.
Savilahti E, Siltanen M, Kajosaari M, Vaarala O, Saarinen KM: IgA antibodies, TGF-beta1 and -beta2, and soluble CD14 in the colostrum and development of atopy by age 4. Pediatr Res 2005;58:1300–1305.
11.
Polte T, Hansen G: Maternal tolerance achieved during pregnancy is transferred to the offspring via breast milk and persistently protects the offspring from allergic asthma. Clin Exp Allergy 2008;38:1950–1958.
12.
Mosconi E, Rekima A, Seitz-Polski B, Kanda A, Fleury S, Tissandie E, Monteiro R, Dombrowicz DD, Julia V, Glaichenhaus N, Verhasselt V: Breast milk immune complexes are potent inducers of oral tolerance in neonates and prevent asthma development. Mucosal Immunol 2010;3:461–474.
13.
Penttila IA: Milk-derived transforming growth factor-beta and the infant immune response. J Pediatr 2010;156:S21–S25.
14.
Verhasselt V, Milcent V, Cazareth J, Kanda A, Fleury S, Dombrowicz D, Glaichenhaus N, Julia V: Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med 2008;14:170–175.
15.
Snijders BE, Damoiseaux JG, Penders J, Kummeling I, Stelma FF, van Ree R, van den Brandt PA, Thijs C: Cytokines and soluble CD14 in breast milk in relation with atopic manifestations in mother and infant (KOALA Study). Clin Exp Allergy 2006;36:1609–1615.
16.
Oddy WH, Rosales F: A systematic review of the importance of milk TGF-beta on immunological outcomes in the infant and young child. Pediatr Allergy Immunol 2010;21:47–59.
17.
Tomicic S, Johansson G, Voor T, Bjorksten B, Bottcher MF, Jenmalm MC: Breast milk cytokine and IgA composition differ in Estonian and Swedish mothers – relationship to microbial pressure and infant allergy. Pediatr Res 2010;68:330–334.
18.
Peroni DG, Pescollderungg L, Piacentini GL, Rigotti E, Maselli M, Watschinger K, Piazza M, Pigozzi R, Boner AL: Immune regulatory cytokines in the milk of lactating women from farming and urban environments. Pediatr Allergy Immunol 2010;21:977–982.
19.
Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M: Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2007;119:192–198.
20.
Kukkonen K, Kuitunen M, Haahtela T, Korpela R, Poussa T, Savilahti E: High intestinal IgA associates with reduced risk of IgE-associated allergic diseases. Pediatr Allergy Immunol 2010;21:67–73.
21.
Savilahti E, Saukkonen TT, Virtala ET, Tuomilehto T, Åkerblom HK: Increased levels of cow’s milk and β-lactoglobulin antibodies in young children with newly diagnosed IDDM. Diabetes Care 1993;16:984–989.
22.
Bruijnzeel-Koomen C, Ortolani C, Aas K, Bindslev-Jensen C, Bjorksten B, Moneret-Vautrin D, Wuthrich B: Adverse reactions to food. European Academy of Allergology and Clinical Immunology Subcommittee. Allergy 1995;50:623–635.
23.
Savilahti E, Tainio VM, Salmenperä L, Arjomaa P, Kallio M, Perheentupa J, Siimes MA: Low colostral IgA associated with cow’s milk allergy. Acta Paediatr Scand 1991;80:1207–1213.
24.
Saarinen KM, Vaarala O, Klemetti P, Savilahti E: Transforming growth factor-beta1 in mothers’ colostrum and immune responses to cows’ milk proteins in infants with cows’ milk allergy. J Allergy Clin Immunol 1999;104:1093–1098.
25.
Fälth-Magnusson K: Breast milk antibodies to foods in relation to maternal diet, maternal atopy and the development of atopic disease in the baby. Int Arch Allergy Appl Immunol 1989;90:297–300.
26.
Böttcher MF, Abrahamsson TR, Fredriksson M, Jakobsson T, Bjorksten B: Low breast milk TGF-beta2 is induced by Lactobacillus reuteri supplementation and associates with reduced risk of sensitization during infancy. Pediatr Allergy Immunol 2008;19:497–504.
27.
Boyle RJ, Ismail IH, Kivivuori S, Licciardi PV, Robins-Browne RM, Mah LJ, Axelrad C, Moore S, Donath S, Carlin JB, Lahtinen SJ, Tang ML: Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial. Allergy 2011;66:509–516.
28.
Prescott SL, Wickens K, Westcott L, Jung W, Currie H, Black PN, Stanley TV, Mitchell EA, Fitzharris P, Siebers R, Wu L, Crane J: Supplementation with Lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin A detection. Clin Exp Allergy 2008;38:1606–1614.
29.
Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E: Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy 2008;38:1342–1348.
30.
Marschan E, Kuitunen M, Kukkonen K, Poussa T, Sarnesto A, Haahtela T, Korpela R, Savilahti E, Vaarala O: Probiotics in infancy induce protective immune profiles that are characteristic for chronic low-grade inflammation. Clin Exp Allergy 2008;38:611–618.
31.
Christensen HR, Frokiaer H, Pestka JJ: Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002;168:171–178.
32.
Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, Zaat BA, Yazdanbakhsh M, Wierenga EA, van Kooyk Y, Kapsenberg ML: Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol 2005;115:1260–1267.
33.
Nakao A: The role and potential use of oral transforming growth factor-beta in the prevention of infant allergy. Clin Exp Allergy 2010;40:725–730.
34.
Oddy WH, Halonen M, Martinez FD, Lohman IC, Stern DA, Kurzius-Spencer M, Guerra S, Wright AL: TGF-beta in human milk is associated with wheeze in infancy. J Allergy Clin Immunol 2003;112:723–728.
35.
Rautava S, Kalliomaki M, Isolauri E: Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol 2002;109:119–121.
36.
Kuitunen M, Kukkonen K, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Haahtela T, Savilahti E: Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J Allergy Clin Immunol 2009;123:335–341.
37.
Prentice A, McCarthy A, Stirling DM, Vasquez-Velasquez L, Ceesay SM: Breast-milk IgA and lactoferrin survival in the gastrointestinal tract – a study in rural Gambian children. Acta Paediatr Scand 1989;78:505–512.
38.
Koutras AK, Vigorita VJ: Fecal secretory immunoglobulin A in breast milk versus formula feeding in early infancy. J Pediatr Gastroenterol Nutr 1989;9:58–61.
39.
Kuitunen M, Savilahti E: Mucosal IgA, mucosal cow’s milk antibodies, serum cow’s milk antibodies and gastrointestinal permeability in infants. Pediatr Allergy Immunol 1995;6:30–35.
40.
Taylor AL, Dunstan JA, Prescott SL: Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol 2007;119:184–191.
41.
Walker A: Breast milk as the gold standard for protective nutrients J Pediatr 2010;156:S3–S7.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.