Immunological programming by breast milk creates an anti-inflammatory cytokine milieu in breast-fed infants compared to formula-fed infants

British Journal of Nutrition

Volumn 109, Issue 11, 2013, Pages 1962-1970

  Kainonen, Essi ^a   Rautava, Samuli ^a   Isolauri, Erika ^a  

^a TURKU UNIVERSITY HOSPITAL   (Finland)

Author keywords

Allergy; Breast milk; Cytokines; Immunology; Infants; Tolerisation; Transforming growth factor

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 5; TRANSFORMING GROWTH FACTOR BETA2; TUMOR NECROSIS FACTOR ALPHA;

ANALYSIS OF VARIANCE; ANTIBODY PRODUCTION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ARTIFICIAL FEEDING; ATOPY; BREAST FEEDING; BREAST MILK; CASE CONTROL STUDY; CLINICAL FEATURE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN EXPERIMENT; IMMUNE SYSTEM; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOLOGY; INFANT; MALE; NORMAL HUMAN; PROTEIN BLOOD LEVEL; QUALITY OF LIFE;

BREAST FEEDING; CASE-CONTROL STUDIES; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULINS; INFANT; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MALE; MILK, HUMAN;

EID: 84877996101     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114512004229     Document Type: Article

References (58)

1. Newburg DS & Walker WA (2007) Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res 61, 2-8.
2. Lonnerdal B (2003) Nutritional and physiologic significance of human milk proteins. Am J Clin Nutr 77, 1537S-1543S.
3. Jeliffe DB & Jeliffe EF (1981) Breast milk and infection. Lancet ii, 419.
4. Ruiz-Palacios GM, Calva JJ, Pickering LK, et al. (1990) Protection of breast-fed infants against Campylobacter diarrhea by antibodies in human milk. J Pediatr 116, 707-713.
5. Clavano NR (1982) Mode of feeding and its effect on infant mortality and morbidity. J Trop Pediatr 28, 287-293.
6. Arifeen S, Black RE, Antelman G, et al. (2001) Exclusive breast-feeding reduces acute respiratory infection and diarrhea deaths among infants in Dhaka slums. Pediatrics 108, E67.
7. Wilson AC, Forsyth JS, Greene SA, et al. (1998) Relation of infant diet to childhood health: seven year follow up of cohort of children in Dundee infant feeding study. BMJ 316, 21-25.
8. Duncan B, Ey J, Halberg CJ, et al. (1994) Exclusive breast feeding for at least 4 months protects against otitis media. Pediatrics 91, 867-872.
9. Golding J, Emmett PM & Rogers IS (1997) Does breast feeding protect against non-gastric infections? Early Hum Dev 29, S105-S120.
10. Kramer MS, Chalmers B, Hodnett ED, et al. (2001) Promotion of Breast-feeding Intervention Trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA 285, 413-420.
11. Rosenbauer J, Herzig P & Giani G (2008) Early infant feeding and risk of type 1 diabetes mellitus-a nationwide population-based case-control study in pre-school children. Diabetes Metab Res Rev 24, 211-222.
12. Barclay AR, Russell RK, Wilson ML, et al. (2009) Systematic review: the role of breast-feeding in the development of pediatric inflammatory bowel disease. J Pediatr 155, 421-426.
13. Akobeng AK, Ramanan AV, Buchan I, et al. (2006) Effect of breast feeding on risk of coeliac disease: a systematic review and meta-analysis of observational studies. Arch Dis Child 91, 39-43.
14. Lucas A, Brooke OG, Morley R, et al. (1990) Early diet in preterm infants and development of allergic or atopic disease: randomized prospective study. BMJ 300, 837-840.
15. Kull I, Wickman M, Lilja G, et al. (2002) Breast-feeding and allergic diseases in infants-a prospective birth study cohort. Arch Dis Child 87, 478-481.
16. Kull I, Almqvist C, Lilja G, et al. (2004) Breast-feeding reduces the risk of asthma during the first 4 years of life. J Allergy Clin Immunol 114, 755-760.
17. Oddy WH, Sly PD, de Klerk NH, et al. (2003) Breast feeding and respiratory morbidity in infancy: a birth cohort study. Arch Dis Child 88, 224-228.
18. Kerkhof M, Koopman LP, van Strien RT, et al. (2003) Risk factors for atopic dermatitis in infants at high risk of allergy: the PIAMA study. Clin Exp Allergy 33, 1336-1341.
19. Lauberau B, Brockow I, Zirngibl A, et al. (2004) Effects of breast-feeding on the development of atopic dermatitis during the first 3 years of life.-results from the GINI-birth cohort study. J Pediatr 144, 602-607.
20. Chandra RK, Puri S & Cheema PS (1985) Predictive value of cord blood IgE in the development of atopic disease and role of breast-feeding in its prevention. Clin Allergy 15, 517-522.
21. Vandenplas Y, Deneyr M, Sacre L, et al. (1988) Preliminary data on a field study with a new hypo-allergenic formula. Eur J Pediatr 148, 274-277.
22. Rautava S & Walker WA (2009) Academy of Breast-feeding Medicine founder's lecture 2008: breast-feeding-an extrau-terine link between mother and child. Breastfeed Med 4, 3-10.
23. Liepke C, Adermann K, Raida M, et al. (2002) Human milk provides peptides highly stimulating the growth of bifido-bacteria. Eur J Biochem 269, 712-718.
24. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, et al. (2000) Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30, 61-67.
25. Friedman NJ & Zeiger RS (2005) The role of breast-feeding in the development of allergies and asthma. J Allergy Clin Immunol 115, 1238-1248.
26. Sears MR, Greene JM, Willan AR, et al. (2002) Long-term relation between breast-feeding and development of atopy and asthma in children and young adults: a longitudinal study. Lancet 360, 901-907.
27. Miyake Y, Yura A & Iki M (2003) Breast-feeding and the prevalence of symptoms of allergic disorders in Japanese adolescents. Clin Exp Allergy 33, 312-316.
28. Bergmann RL, Diepgen TL, Kuss O, et al. (2002) Breastfeeding duration is a risk factor for atopic eczema. Clin Exp Allergy 32, 205-209.
29. Taylor B, Wadsworth J, Golding J, et al. (1983) Breastfeeding, eczema, asthma and hayfever. J Epidemiol Community Health 37, 95-99.
30. Kaplan BA & Mascie-Taylor CG (1985) Biosocial factors in the epidemiology of childhood asthma in a British national sample. J Epidemiol Community Health 39, 152-156.
31. Rusconi F, Galassi C, Corbo GM, et al. (1999) Risk factors for early, persistent and late onset wheezing in young children. SIDRIA Collaborative Group. Am J Respir Crit Care Med 160, 1617-1622.
32. Li MO, Wan YY, Sanjabi S, et al. (2006) Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24, 99-146.
33. + Th1/Th2 T cells. Eur J Immunol 30, 2101-2111.
34. Takeuchi M, Alard P & Streilein JW (1998) TGF-beta promotes immune deviation by altering accessory signals of antigen-presenting cells. J Immunol 160, 1589-1597.
35. + regulatory T cell activity in both humans and mice. J Immunol 172, 834-842.
36. Ogawa J, Sasahara A, Yoshida T, et al. (2004) Role of transforming growth factor-beta in breast milk for initiation of IgA production in newborn infants. Early Hum Dev 77, 67-75.
37. Verhasselt V, Milcent V, Cazareth J, et al. (2008) Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med 14, 170-175.
38. Penttila I (2006) Effects of transforming growth factor-beta and formula feeding on systemic immune responses to dietary beta-lactoglobulin in allergy-prone rats. Pediatr Res 59, 650-655.
39. Sanders DS (2005) Mucosal integrity and barrier function in the pathogenesis of early lesions in Crohn's disease. J Clin Pathol 58, 568-572.
40. Desjeux JF & Heyman M (1994) Milk proteins, cytokines and intestinal epithelial functions in children. Acta Paediatr Jpn 36, 592-596.
41. Letterio JJ, Geiser AG, Kulkarni AB, et al. (1994) Maternal rescue of transforming growth factor-beta 1 null mice. Science 264, 1936-1938.
42. Ando T, Hatsushika K, Wako M, et al. (2007) Orally administered TGF-beta is biologically active in the intestinal mucosa and enhances oral tolerance. J Allergy Clin Immunol 120, 916-923.
43. Jones CA, Holloway JA, Popplewell EJ, et al. (2002) Reduced soluble CD14 levels in amniotic fluid and breast milk are associated with the subsequent development of atopy, eczema, or both. J Allergy Clin Immunol 109, 858-866.
44. Laiho K, Lampi AM, Hamalainen M, et al. (2003) Breast milk fatty acids, eicosanoids, and cytokines in mothers with and without allergic disease. Pediatr Res 53, 642-647.
45. Hoppu U, Kalliomaki M, Laiho K, et al. (2001) Breast milk- immunomodulatory signals against allergic diseases. Allergy 56, 23-26.
46. Kalliomaki M, Ouwehand A, Arvilommi H, et al. (1999) Transforming growth factor-beta in breast milk: a potential regulator of atopic disease at an early age. Allergy Clin Immunol 104, 1251-1257.
47. Gueimonde M, Laitinen K, Salminen S, et al. (2007) Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology 92, 64-66.
48. Donnet-Hughes A, Perez PF, Doré J, et al. (2010) Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc 69, 407-415.
49. Abrahamsson TR, Sinkiewicz G, Jakobsson T, et al. (2009) Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr 49, 349-354.
50. LeBouder E, Rey-Nores JE, Raby AC, et al. (2006) Modulation of neonatal microbial recognition: TLR-mediated innate immune responses are specifically and differentially modulated by human milk. J Immunol 176, 3742-3752.
51. Chichlowski M, German JB, Lebrilla CB, et al. (2011) The influence of milk oligosaccharides on microbiota of infants: opportunities for formulas. Annu Rev Food Sci Technol 2, 331-351.
52. Bakker-Zierikzee AM, Alles MS, Knol J, et al. (2005) Effects of infant formula containing a mixture of galacto-and fructo-oligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. Br J Nutr 94, 783-790.
53. Asakuma S, Hatakeyama E, Urashima T, et al. (2011) Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem 286, 34583-34592.
54. Sela DA, Chapman J, Adeuya A, et al. (2008) The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105, 18964-18969.
55. Kaila M, Arvilommi H, Soppi E, et al. (1994) A prospective study of humoral immune responses to cow milk antigens in the first years of life. Pediatr Allergy Immunol 5, 164-169.
56. Tainio VM, Savilahti E, Arjomaa P, et al. (1988) Plasma antibodies to cow's milk are increased by early weaning and consumption of unmodified milk, but production of plasma IgA and IgM cow's milk antibodies is stimulated even during exclusive breast-feeding. Acta Paediatr Scand 77, 807-811.
57. Vaarala O, Saukkonen T, Savilahti E, et al. (1995) Development of immune response to cow's milk proteins in infants receiving cow's milk or hydrolysed formula. J Allergy Clin Immunol 96, 917-923.
58. Jenmalm MC & Björksten B (1998) Exposure to cow's milk during the first 3 months of life is associated with increased levels of IgG antibodies to beta-lactoglobulin up to 8 years. J Allergy Clin Immunol 102, 671-678.