This paper is only available as a PDF. To read, Please Download here.
Objectives
The reader of this review will learn about the mechanisms through which breastfeeding
protects against infections during and most likely after lactation, as well as possibly
against certain immunologic diseases, including allergy.
Data sources
I have followed the literature in the area closely for the last 30 to 40 years and
have made repeated literature searches through MEDLINE, most recently in 1998. Textbooks
and peer-reviewed journals have been sought for, as well as books representing meeting
reports in English, French, German, and Spanish.
Results
Human milk protects against infections in the breastfed offspring mainly via the secretory
IgA antibodies, but also most likely via several other factors like the bactericidal
lactoferrin. It is striking that the defense factors of human milk function without
causing inflammation, some components are even directly antiinflammatory. Protection
against infections has been well evidenced during lactation against, eg, acute and
prolonged diarrhea, respiratory tract infections, otitis media, urinary tract infection,
neonatal septicemia, and necrotizing enterocolitis. There is also interesting evidence
for an enhanced protection remaining for years after lactation against diarrhea, respiratory
tract infections, otitis media, Haemophilus influenzae type b infections, and wheezing illness. In several instances the protection seems
to improve with the duration of breastfeeding. Some, but not all studies have shown
better vaccine responses among breastfed than non-breastfed infants.
A few factors in milk like anti-antibodies (anti-idiotypic antibodies) and T and B
lymphocytes have in some experimental models been able to transfer priming of the
breastfed offspring. This together with transfer of numerous cytokines and growth
factors via milk may add to an active stimulation of the infant's immune system. Consequently,
the infant might respond better to both infections and vaccines. Such an enhanced
function could also explain why breastfeeding may protect against immunologic diseases
like celiac disease and possibly allergy. Suggestions of protection against autoimune
diseases and tumors have also been published, but need confirmation.
Conclusions
Breastfeeding may, in addition to the well-known passive protection against infections
during lactation, have a unique capacity to stimulate the immune system of the offspring
possibly with several long-term positive effects
To read this article in full you will need to make a payment
ACAAI Member Login
ACAAI Member, full access to the journal is a member benefit. Use your society credentials to access all journal content and features.
Already a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
REFERENCES
- Comparative immunological studies of the immune globulins of human milk and blood serum.Int Archs Allergy Appl Immun. 1961; 18: 241-267
- The mucosal defense system.in: Stiehm RT Immunologic Disorders in Infants & Children. Fourth edition. Saunders, Philadelphia1996: 159-199
Goldman AS. The immunological system in human milk: the past—a pathway to the future. In: Advances in Nutritional Research. Woodward, WH, Draper, HH (eds). Plenum Press. 1998, vol. 10, pp. in press.
- Anti-inflammatory properties of human milk.Acta Paediatr Scand. 1986; 75: 689-694
- Cytokines in human milk.Res Comm Molecul Pathol Pharmacol. 1996; 93: 263-287
- Isolation of interleukin-1 from human milk.Int Arch All Appl Immunol. 1987; 83: 19-23
- Presence of interferon-gamma and interleukin-6 in colostrum of normal women.Cytokine Research. 1993; 12: 21-24
- Tumor necrosis factor-α in human milk.Paediatric Research. 1992; 31: 29-33
- Cytokine production in mononuclear cells of human milk studies at the single-cell level.Pediatric Research. 1993; 34: 213-216
- Lactoferrin or a fragment thereof inhibits the endotoxin-induced interleukin-6 response in human monocytic cells.Pediatr Res. 1996; 40: 257-262
Ceafalau L, Hahn-Zoric M, Hanson LÅ, et al. Lactoferrin inhibits the LPS-induced expression of IL-6 mRNA in THP-1 cells. Third International Conference on Lactoferrin Structure and Function, 1997.
- Molecular cloning and expression of a pituitary gland protein modulating intestinal fluid secretion.J Biol Chem. 1995; 270: 20615-20620
- Anti-piliantibodies in breast milk.Lancet. 1979; ii: 1235
- Anti-adhesive activity of human casein against Streptococcus pneumoniae and Haemophilus influenzae.Microb Pathogen. 1990; 8: 315-323
- Inhibition of attachment of Streptococcus pneumoniae and Haemophilus influenzae by human milk and receptor oligosaccharides.J Infect Dis. 1986; 153: 232-237
- Nonimmunoglobulin fraction of human milk inhibits bacterial adhesion (hemagglutination) and enterotoxin binding of Escherichia coli and Vibrio cholerae.Infect Immun. 1981; 33: 136
- Inhibition of enterotoxin from Escherichia coli and Vibrio cholerae by gangliosides from human milk.Infect Immun. 1983; 40: 563
- Inhibition of localized adhesion of enteropathogenic Escherichia coli to Hep-2 cells by immunoglobulin and oligosaccharide fractions of human colostrum and breast milk.J Infect Dis. 1991; 163: 1247-1255
- Fucosylated oligosaccharides of human protect suckling mice from heat-stabile enterotoxin of Escherichia coli.J Infect Dis. 1990; 162: 1075-1080
Ruiz-Palacios GM, Cervantes LE, Newburg DS, et al. In vitro models for studying Campylobacter jejuni infections. In: Campylobacter jejuni. Current Status and Future Trends. Nachamkin, I, Blaser, MJ, Tomkins, LS (eds). American Society for Microbiology. Washington, DC. 1992, in press.
- Protection against cholera in breast-fed children by antibodies in breast-milk.N Engl J Med. 1983; 308: 1389-1392
- Breast-milk anti-Escherichia coli heat-labile toxin IgA antibodies protect against toxin-induced infantile diarrhoea.Acta Paediatr Scand. 1988; 77: 658-662
- Protection of breast-fed infants against Campylobacter diarrhoea by antibodies in human milk.J Pediatr. 1990; 116: 707-713
- Interventions for the control of diarrhoeal diseases among young children: promotion of breast-feeding.Bull WHO. 1984; 62: 271-291
- Protective effect of breast feeding against infection.BMJ. 1990; 300: 11-16
- The effects of infant feeding on rotavirus-induced gastroenteritis: A prospective study.Am J Publ Health. 1986; 76: 259-263
- Breast-feeding and the risk of life-threatening rotavirus diarrhea: Prevention or postponement?.Pediatrics. 1993; 92: 680-685
- Rotavirus infections in young Nicaraguan children.Pediatr Infect Dis J. 1997; 16: 564-571
- Role of human-milk lactadherin in protection against symptomatic rotavirus infection.Lancet. 1998; 351: 1160-1164
- Breast-feeding and lower respiratory tract illness in the first year of life.BMJ. 1989; 299: 946-949
- Prolonged breast feeding as prophylaxis for recurrent otitis media.Acta Pediatr Scand. 1982; 71: 567-571
- Exclusive breast-feeding for at least 4 months protects against otitis media.Pediatrics. 1993; 91: 867-872
- Breast feeding and toxigenic intestinal infections: missing links in crib death?.Rev Infect Dis. 1984; 6: 193-201
- Breast milk and neonatal necrotising enterocolitis.Lancet. 1990; 336: 1519-1523
- Working Group on Breastfeeding: Science and Society.Pontificiae Academiae Scientiarum Documenta. 1995; 20: 1-33
- Medical histories of children with acute pyelonephritis compared with controls.Pediatr Infect Dis J. 1989; 8: 511-515
- Breastfeeding and urinary-tract infection.Lancet. 1990; 336: 942
- Breastfeeding and urinary tract infection.J Pediatr. 1992; 120: 87-89
- Breastfeeding and biological properties of faecal Escherichia coli strains.Acta Paediatr Scand. 1975; 64: 807-812
Slàviková M, Lòdinová-Zàdniková R, Adlerberth I, et al. Breast-feeding enhances the expression of type 1 fimbriae by E. coli in the gut of the newborn infant. J Inf Dis 1998, in press.
- Fecal colonization with P-fimbriated Escherichia coli between 0 and 18 months of age.Epdemiol Infect. 1988; 100: 185-191
- Preliminary study of breastfeeding and bacterial adhesion to uroepithelial cells.Lancet. 1990; 335: 569-571
- Urinary excretion of lactose and oligosaccharides in preterm infants fed human milk or infant formula.Acta Paediatr. 1996; 85: 598-603
- Defense factors in human milk.Curr Opin Gastroenterol. 1994; 10: 652-658
- Human milk feeding enhances the urinary excretion of immunologic factors in low birth weight infants.Pediatr Res. 1989; 25: 184-188
- Breastfeeding and protection against neonatal sepsis in a high risk population.Arch Dis Child. 1991; 66: 488-490
- Does breast milk protect against septicaemia in the newborn?.Lancet. 1971; 1: 1091-1094
- Evidence for protection by breast-feeding against infant deaths from infectious diseases in Brazil.Lancet. 1987; ii: 319-322
- Relation of infant diet to childhood health: seven year follow up of cohort of children in Dundee infant feeding study. 1998; 316: 21-25
- Breast feeding and acute lower respiratory infection.Acta Paediatr. 1994; 83: 714-718
- Breastfeeding and the use of human milk.Pediatrics. 1997; 100: 1035-1039
Hanson LÅ, Telemo E. Immunobiology and epidemiology of breast feeding in relation to prevention of infections from a global perspective. In: Ogra, PL, Strober, W, Bienenstock, J (eds). Mucosal Immunology. Academic Press. 1998, in press.
- Protective effect of breastfeeding on invasive Haemophilus influenzae infection: A case-control study in Swedish preschool children.Int J Epidemiol. 1997; 26: 443-450
Silfverdal SA, Bodin L, Olcén P. Protection of breastfeeding on a population level: An ecological study on the incidence of Haemophilus influenzae meningitis in a Swedish population in relation to contemporary breastfeeding-rates. Submitted, 1998.
- Early wheezing and breast feeding.Asthma. 1993; 30: 23-28
- Infant feeding, wheezing, and allergy: a prospective study.Arch Dis Child. 1993; 68: 724-728
- Community study of role of viral infections in exacerbations of asthma in 9–11 year old children.BMJ. 1995; 310: 1225-1229
- Parental smoking and other risk factors for wheezing bronchitis in children.Eur J Epidemiol. 1993; 9: 517-526
- Breast feeding and acute appendicitis.BMJ. 1995; 310: 836-837
- Breast feeding and tonsillectomy.BMJ. 1996; 312: 746-747
- Effect on breast-feeding on antibody response to BCG vaccination.Lancet. 1989; 1: 295-297
- Antibody responses to parenteral and oral vaccines are impaired by conventional and low protein formulas as compared to breast-feeding.Acta Paediatr Scand. 1990; 79: 1137-1142
- Immunogenicity of Haemophilus influenzae type b tetanus toxoid conjugate vaccine in young infants.J Infect Dis. 1994; 170: 76-81
- Modulation of the immune system by human milk and infant formula containing nucleotides.Pediatrics. 1998; 101: 242-249
- Effect of breastfeeding on oral rhesus rotavirus vaccine seroconversion: a metaanalysis.J Infect Dis. 1990; 162: 753-755
- Factors affecting the immunogenicity of oral poliovirus vaccine: A prospective evaluation in Brazil and Gambia.J Infect Dis. 1995; 171: 1097-1106
- Safety and immunogenicity of a cold-adapted influenza A (H1N1) reassortant virus vaccine administered to infants less than six months of age.Pediatr Infect Dis J. 1995; 14: 10-16
- Influence of breastfeeding and oral poliovirus vaccine on the immunogenicity and efficacy of rotavirus vaccines.J Infect Dis. 1996; 174: 107-111
- Safety and immunogenicity of Haemophilus type b-tetanus protein conjugate vaccine, mixed in the same syringe with diphtheria-tetanus-pertussis vaccine in young infants.Pediatr Infect Dis J. 1991; 10: 758-761
- Breastfeeding and antibody responses to routine vaccination in infants.Lancet. 1992; 340: 1406
- Comparative trial in infants of four conjugate Haemophilus influenzae type b vaccines.J Pediatr. 1992; 120: 184-189
- In vivo immune responses of breast- and bottle-fed infants to tetanus toxoid antigen and to normal gut flora.Acta Paediatr Scand. 1984; 73: 426-432
Lundin S, Dahlman-Hoglund A, Pettersson I, et al. Antibodies given orally in the neonatal period can affect the immune response for two generations: evidence for active maternal influence on the newborn's immune system. Submitted 1998.
- Phenotype of T cells, their soluble receptor levels, and cytokine profile of human breast milk.Immunol Cell Biol. 1994; 72: 306-313
- Postnatal changes in mucosal immune response: A physiological perspective of breast feeding and weaning. Review Article.Immunol Cell Biol. 1997; 75: 419-429
- Effects of milk-borne colony stimulating factor-1 on circulating growth factor levels in the newborn infant.J Pediatr. 1997; 131: 748-750
- Maternal rescue of transforming growth factor-β null mice.Science. 1994; 264: 1936-1938
- Soluble tumor necrosis factor-α (TNF-a) receptors in human colostrum and milk bind to TNF-α and neutralize TNF-α bioactivity.Pediatric Research. 1998; 44: 37-42
- Effect of breast-feeding on responses of systemic interferon and virus-specific lymphocyte transformation in infants with respiratory syncytical virus infection.J Med Virol. 1987; 21: 7-14
- Differential modulation of the immune response by breast- or formula-feeding of infants.Acta Paediatr. 1997; 86: 1291-1297
- Neonatal administration of idiotype or anti-idiotype primes for protection against Escherichia coli K13 infection in mice.J Exp Med. 1984; 160: 1001-1011
- Effect of breast feeding on the development of anti-idiotype antibody response to F glycoprotein of respiratory syncytial virus in infant mice after post-partum maternal immunization.J Immunol. 1989; 142: 2507-2512
- Anti-idiotypic antibodies to poliovirus in commercial immuno-globulin, human serum and human milk.Pediatr Res. 1993; 33: 475-480
- Demonstration that milk cells invade the suckling neonatal mouse.Am J Reproduct Immunol. 1983; 4: 95-98
- Intestinal uptake of intact maternal lymphocytes by neonatal rats and lambs.Res Vet Science. 1985; 39: 10-15
- In vivo distribution of human milk leucocytes after ingestion by newborn baboons.Arch Dis Child. 1989; 64: 930-933
Siafakas C, Anderson W, Walker A, et al. Breast milk cells and their interaction with intestinal mucosa. In: Third Neonatal Hematology and Immunology Symposium. Bellanti, J, Brain, R, Prindull, G, et al. (eds). Elsevier Science Publishers. Amsterdam. 1998, in press.
- Intestinal absorption of colostral lymphocytes in newborn lambs and their role in the development of immune status.Acta Vet Hungar. 1995; 43: 105-115
- Maternal to neonatal transmission of T-cell mediated immunity to Trichinella spiralis during lactation.Immunology. 1989; 68: 87-92
- Breast feeding and maternal-donor renal allografts. Possibly the original donor-specific transfusion.Transplantation. 1984; 37: 340-344
- Influence of breast feeding on subsequent reactivity to a related renal allograft.J Surg Research. 1984; 37: 89-93
- Regulation of parental alloreactivity by reciprocal F1 hybrids. The role of lactation.J Reprod Immunol. 1993; 23: 235-245
- Influence of breast feeding on the cytotoxic T cell allorepertoire in man.Transplantation. 1991; 52: 914-916
Gustafsson E, Arvola M, Svensson L, et al. Postnatally transmitted maternal B cells can cause long-term maintenance of serum IgG in B cell-deficient mice nursed by phenotypically normal dams. Submitted, 1998.
- Evidence for transmission of lymphocyte responses to tuberculin by breastfeeding.Lancet. 1977; ii: 529-532
- Immunologic aspects of human colostrum and milk. III. Fate and absorption of cellular and soluble components in the gastrointestinal tract of the newborn.J Immunol. 1977; 119: 245-248
- Transfer of tuberculin immunity from mother to infant.Pediatr Res. 1987; 22: 277-281
- Dietary nucleotide effects upon immune function in infants.Pediatrics. 1991; 88: 359-363
- Decreased thymus size in formula-fed infants compared with breastfed infants.Acta Paediatr. 1996; 85: 1029-1032
- Regulatory feedback pathways in the thymus.Immunol Today. 1997; 18: 581-585
- Does breast feeding protect against the development of clinical symptoms of celiac disease in children?.J Pediatr Gastroenterol Nutr. 1983; 2: 428-433
- Case control study on nutritional risk factors in celiac disease.J Gastroenterol Nutr. 1988; 7: 395-399
- Infant feeding history shows distinct differences between Swedish coeliac and reference children.Pediatr Allergy Immunol. 1996; 7: 1-5
Ivarsson A, Persson LÅ, Hernell O. Risk factors for coeliac disease in childhood: A report from the Swedish multicenter study. 1998, in manuscript.
- Role of infant feeding practices in development of Crohn's disease in childhood.BMJ. 1989; 298: 1617-1618
- Infant feeding practices and ulcerative colitis in childhood.BMJ. 1991; 302: 1580-1581
- The growing allergy problem. (Invited commentary).Acta Paediatr. 1997; 86: 916-918
- Prospective studies of the effect of breast feeding on incidence of infection and allergy.Acta Paediatr Scand. 1979; 68: 691-694
- Prolonged breast-feeding as prophylaxis for atopic disease.Lancet. 1979; ii: 163-168
- Prevention of atopic disease in “at-risk newborns” by prolonged breast-feeding.Ann Allergy. 1983; 51: 296-299
- Effect of combined maternal and infant food-allergen avoidance on development of atopy in early infancy: A randomized study.J Allergy Clin Immunol. 1989; 84: 72-89
- Clinical manifestations of allergy related to breast and cows' milk feeding.Arch Dis Child. 1981; 56: 172-175
- Breast feeding and eczema/asthma.Lancet. 1982; i: 910
- Relationship of diet in the development of atopy in infancy.Clin Allergy. 1984; 14: 525-532
- The prevalence of allergic diseases in primary school children in Edirne, Turkey.Clin Exp Allergy. 1997; 27: 262-269
Hesselmar B, Åberg N, Åberg B, et al. Does early exposure to cat and dog protect against later allergy development? 1998, submitted.
- Breastfeeding as prophylaxis against atopic disease.Lancet. 1995; 346: 1714
- Breastfeeding as prophylaxis against atopic disease: prospective follow-up study until 17 years old.Lancet. 1995; 346: 1065-1069
- Effectiveness of dietary manipulation in the prevention of food allergy in infants.J Allergy Clin Immunol. 1986; 78: 224-238
- Does breast feeding help protect against atopic disease? Biology, methodology, and a golden jubilee of controversy.J Pediatr. 1988; 112: 181-190
- Effect of maternal avoidance of eggs, cow's milk and fish during lactation upon allergic manifestations in infants.Clin Exp Allergy. 1989; 19: 27-32
- Maternal avoidance of eggs, cow's milk, and fish during lactation: effect on allergic manifestations, skin-prick tests, and specific IgE antibodies in children at age 4 years.Pediatrics. 1992; 89: 735-739
- Dietary factors influencing levels of food antibodies and antigens in breast milk.Acta Paediatr. 1996; 85: 778-784
- Sensitization via the breast milk.in: Ogra PL Strober W Mestecky J Adv Exp Med Biol. vol. 310. Plenum Press, New York1991: 427-436
- 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
- Maternal immune status against beta-lactoglobulin and cow milk allergy in the infant.Ann Allergy. 1989; 63: 517-519
- 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
- Preventive effect of feeding high-risk infants a casein hydrolysate formula or an ultrafiltrated whey hydrolysate formula. A prospective, randomized, comparative clinical study.Pediatr Allergy Immunol. 1993; 4: 173-181
- The long-term effect of a partial whey hydrolysate formula on the prophylaxis of atopic disease.Eur J Pediatr. 1995; 154: 488-494
- Effects of a dietary and environmental prevention programme on the incidence of allergic symptoms in high atopic risk infants: three years follow-up.Acta Paediatr Suppl. 1996; 414: 1-22
- Induction of systemic immunologic tolerance to beta-lactoglobulin by oral administration of a whey protein hydrolysate.J Allergy Clin Immunol. 1997; 100: 266-273
- Extensively and partially hydrolysed infant formulas for allergy prophylaxis.Arch Dis Childhood. 1997; 77: 4-10
- Early diet of preterm infants and development of allergic or atopic disease: randomised prospective study.BMJ. 1990; 300: 837-840
- Hydrolysed cow's milk formulae. Allergenicity and use in treatment and prevention. An ESPACI position paper.Pediatr Allergy Immunol. 1993; 4: 101-111
- Breast milk from mothers of children with newly developed atopic eczema has low levels of long chain polyunsaturated fatty acids.J Allergy Clin Immunol. 1993; 91: 1134-1139
Duchén K, Yu G, Björkstén B. Atopic sensitisation during the first year of life in relation to long chain polyunsaturated fatty acid levels in human milk. 1998, submitted.
- The genetics and complexity of allergy and asthma.Immunol Today. 1998; 19: 325-332
- Relation between breast-feeding and incidence rates of insulin-dependent diabetes mellitus.Lancet. 1984; i: 1083-1086
- Breast feeding and insulin-dependent diabetes mellitus in children.J Am Coll Nutr. 1986; 5: 439-441
- Reduced risk of IDDM among breastfed children.Diabetes. 1988; 37: 1625-1632
- Breastfeeding and the risk of sudden infant death syndrome.Int J Epidemiol. 1993; 22: 885-890
- Infant feeding in Finnish children <7 yr of age with newly diagnosed IDDM.Diabetes Care. 1991; 14: 415-417
- Feeding in infancy and the risk of type 1 diabetes mellitus in Finnish children.Diabetic Medicine. 1992; 9: 815-819
- An immunological basis for disproportionate diabetes risks in children with a type I diabetic mother or father.Diabetes Care. 1993; 16: 949-951
- A meta-analysis of infant diet and insulin-dependent diabetes mellitus: Do biases play a role?.Epidemiology. 1995; 7: 87-92
- Cow's milk exposure and type 1 diabetes mellitus.Diabetes Care. 1994; 17: 13-19
- Early infant diets and insulin-dependent diabetes.Lancet. 1996; 347: 1464-1465
- Cow milk feeding induces antibodies to insulin in children—a link between cow milk and insulin-dependent diabetes mellitus?.Scand J Immunol. 1998; 47: 131-135
- Breastfeeding and incidence of non-insulin-dependent diabetes mellitus in Pima Indians.Lancet. 1997; 350: 166-168
- Breast feeding and multiple sclerosis.BMJ. 1994; 308: 1411-1412
- Breast feeding, other reproductive factors and rheumatoid arthritis. A prospective study.Br J Rheumatol. 1995; 34: 542-546
- Breast and soy-formula feedings in early infancy and the prevalence of autoimmune thyroid disease in children.J Am Coll Nutr. 1990; 9: 164-167
- Infant feeding and childhood cancer.Lancet. 1988; ii: 365-368
- An exploratory study of environmental and medical factors potentially related to childhood cancer.Med Ped Oncology. 1991; 19: 115-121
Davis MK. Review of the evidence of an association between infant feeding and childhood cancer. 1998, in manuscript.
Article Info
Publication History
Accepted:
September 29,
1998
Received:
June 12,
1998
Footnotes
Supported by an unrestricted grant from Zenica Pharmaceuticals
Supported by a grant by The Swedish Medical Research Council (No 215) , the Hesselman and Vårdal Foundations.
Identification
Copyright
© 1998 American College of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.
