Breastfeeding: maintaining an irreplaceable immunological resource

Abstract

Breastfeeding — the main source of active and passive immunity in the vulnerable early months and years of life — is considered to be the most effective preventive means of reducing the death rate of children under five. Given this, one must wonder why it has slipped quietly down the priorities of the global health and development agendas. In this era of public–private partnerships, can its role as an irreplaceable immunological resource help keep it at the top of global agendas?

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Jones, G. et al. How many child deaths can we prevent this year? Lancet 362, 65–71 (2003).

    PubMed  PubMed Central  Google Scholar 

  2. 2

    Dewey, K. G. Cross-cultural patterns of growth and nutritional status of breast-fed infants. Am. J. Clin. Nutr. 67, 10–17 (1998).

    CAS  PubMed  Google Scholar 

  3. 3

    Anderson, J. W., Johnstone, B. M. & Remley, D. T. Breast-feeding and cognitive development: a meta-analysis. Am. J. Clin. Nutr. 70, 525–535 (1999).

    CAS  PubMed  Google Scholar 

  4. 4

    Goldman, A. S., Chheda, S. & Garofalo, R. Evolution of immunological functions of the mammary gland and the postnatal development of immunity. Pediatr. Res. 43, 155–162 (1998).

    CAS  PubMed  Google Scholar 

  5. 5

    Goldman, A. S. Modulation of the gastrointestinal tract of infants by human milk. Interfaces and interactions. An evolutionary perspective. J. Nutr. 130, 426S–431S (2000).

    CAS  PubMed  Google Scholar 

  6. 6

    Goldman, A. S. Evolution of the mammary gland defense system and ontogeny of the immune system. J. Mammary Gland Biol. Neoplasia 7, 277–289 (2002).

    PubMed  Google Scholar 

  7. 7

    Hanson, L. et al. The immunological role of breast feeding. Pediatr. Allergy Immunol. 12, 15–19 (2001).

    PubMed  Google Scholar 

  8. 8

    Goldman, A., Chheda, S. & Keeney, S. E. in Fetal and Neonatal Physiology 3rd edn Vol. 2 Ch. 184 (eds Polin, R. A., Fox, W. W. & Abman, S. H.) 2022–2032 (Elsevier, Philadelphia, 2002).

    Google Scholar 

  9. 9

    Smith, H. W. & Crabb, W. E. The fecal bacterial flora of animals and man: its development in the young. J. Pathol. Bacteriol. 82, 53–66 (1961).

    Google Scholar 

  10. 10

    György, P., Jeanloz, R. W., von Nicolai, H. & Zilliken, F. Undialyzable growth factors for Lactobacillus bifidus var. Pennsylvanicus. Protective effect of sialic acid bound to glycoproteins and oligosaccharides against bacterial degradation. Eur. J. Biochem. 43, 29–33 (1974).

    PubMed  Google Scholar 

  11. 11

    Bezkorovainy, A. & Topouzian, N. Bifidobacterium bifidus var. Pennsylvanicus growth promoting activity of human milk casein and its derivatives. Int. J. Biochem. 13, 585–590 (1981).

    CAS  PubMed  Google Scholar 

  12. 12

    Liepke, C. et al. Human milk provides peptides highly stimulating the growth of bifidobacteria. Eur. J. Biochem. 269, 712–718 (2002).

    CAS  PubMed  Google Scholar 

  13. 13

    Norton, R. C. & Shohl, A. T. The hydrogen ion concentration of the stools of newborn infants. Am. J. Dis. Child. 32, 183–191 (1926).

    CAS  Google Scholar 

  14. 14

    Fransson, G. B. & Lonnerdal, B. Iron in human milk. J. Pediatr. 96, 380–384 (1980).

    CAS  PubMed  Google Scholar 

  15. 15

    Yamauchi, K., Tomita, M., Giehl, T. J. & Ellison, R. T. Antibacterial activity of lactoferrin and a pepsin-derived lactoferrin peptide fragment. Infect. Immun. 61, 719–728 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Goldman, A. S., Garza, C., Schanler, R. J. & Goldblum, R. M. Molecular forms of lactoferrin in stool and urine from infants fed human milk. Pediatr. Res. 27, 252–255 (1990).

    CAS  PubMed  Google Scholar 

  17. 17

    Boat, T. F., Kleinerman, J. I., Fanaroff, A. A. & Stern, R. C. Human tracheobronchial secretions: development of mucous glycoprotein and lysozyme-secreting systems. Pediatr. Res. 11, 977–980 (1977).

    CAS  PubMed  Google Scholar 

  18. 18

    Hanson, L. A. et al. Neonatal colonization with Escherichia coli and the ontogeny of the antibody response. Prog. Allergy 33, 40–52 (1983).

    CAS  PubMed  Google Scholar 

  19. 19

    Lindh, E. Increased resistance of immunoglobulin dimers to proteolytic degradation after binding of secretory component. J. Immunol. 114, 284–286 (1975).

    CAS  PubMed  Google Scholar 

  20. 20

    Goldman, A. S. & Goldblum, R. M. in Protein and Non-protein Nitrogen in Human Milk (eds Atkinson, S. A. & Lonnerdal, B.) 43–51 (CRC, Boca Raton, 1989).

    Google Scholar 

  21. 21

    Gilbert, J. V., Plaut, A. G., Longmaid, B. & Lamm, M. E. Inhibition of bacterial IgA proteases by human secretory IgA and serum. Ann. NY Acad. Sci. 409, 625–636 (1983).

    CAS  PubMed  Google Scholar 

  22. 22

    Laegreid, A. & Kolsto Otnaess, A. B. Trace amounts of ganglioside GM1 in human milk inhibit enterotoxins from Vibrio cholerae and Escherichia coli. Life Sci. 40, 55–62 (1987).

    CAS  PubMed  Google Scholar 

  23. 23

    Newburg, D. S., Ashkenazi, S. & Cleary, T. G. Human milk contains the Shiga toxin and Shiga-like toxin receptor glycolipid Gb3. J. Infect. Dis. 166, 832–836 (1992).

    CAS  PubMed  Google Scholar 

  24. 24

    Schroten, H. in Advances in Nutritional Research Vol. 10 (eds Woodward, B. & Draper, H. H.) 231–245 (Plenum, New York, 2001).

    Google Scholar 

  25. 25

    Schroten, J. et al. Inhibition of adhesion of S-fimbriated Escherichia coli to buccal epithelial cells by human milk fat globule membrane components: a novel aspect of the protective function of mucins in the nonimmunoglobulin fraction. Infect. Immun. 60, 2893–2899 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Newburg, D. et al. Role of human-milk lactadhedrin in protection against symptomatic rotavirus infection. Lancet 351, 1160–1164 (1998).

    CAS  PubMed  Google Scholar 

  27. 27

    Issacs, C. E. in Advances in Nutritional Research. Vol. 10 (eds Woodward, B. & Draper, H. H.) 271–285 (Plenum, New York, 2001).

    Google Scholar 

  28. 28

    Wirt, D. P., Adkins, L. T., Palkowetz, K. H., Schmalstieg, F. C. & Goldman, A. S. Activated and memory T lymphocytes in human milk. Cytometry 13, 282–290 (1992).

    CAS  PubMed  Google Scholar 

  29. 29

    Pabst, H. F., Godel, J., Grace, M., Cho, H. & Spady, D. W. Effect of breast-feeding on immune response to BCG vaccination. Lancet 1, 295–297 (1989).

    CAS  PubMed  Google Scholar 

  30. 30

    Goldman, A. S., Goldblum, R. M. & Hanson, L. A. in Antioxidant Nutrients and the Immune Response (eds Bendich, A., Phillips, M. & Tengerdy, R.) 69–76 (Plenum, New York, 1989).

    Google Scholar 

  31. 31

    Park, P. W., Biedermann, K., Mecham, L., Bissett, D. L. & Mecham, R. P. Lysozyme binds to elastin and protects elastin from elastase-mediated degradation. J. Invest. Dermatol. 106, 1075–1080 (1996).

    CAS  PubMed  Google Scholar 

  32. 32

    Garofalo, R. et al. Interleukin-10 in human milk. Pediatr. Res. 37, 444–449 (1995).

    CAS  PubMed  Google Scholar 

  33. 33

    Saito, S., Yoshida, M., Ichijo, M., Ishizaka, S. & Tsujii, T. Transforming growth factor-β (TGF-β) in human milk. Clin. Exp. Immunol. 94, 220–224 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Buescher, E. S. & McWilliams-Koeppen, P. Soluble tumor necrosis factor-α (TNF-α) receptors in human colostrum and milk bind to TNF-α and neutralize TNF-α bioactivity. Pediatr. Res. 44, 37–42 (1998).

    CAS  PubMed  Google Scholar 

  35. 35

    Biol, M. C., Pintori, S., Mathian, B. & Louisot, P. Dietary regulation of intestinal glycosyl-transferase activities: relation between developmental changes and weaning in rats. J. Nutr. 121, 114–125 (1991).

    CAS  PubMed  Google Scholar 

  36. 36

    Shulman, R. J. et al. Early feeding, antenatal glucocorticoids, and human milk decrease intestinal permeability in preterm infants. Pediatr. Res. 44, 519–534 (1998).

    CAS  PubMed  Google Scholar 

  37. 37

    Chiba, Y. et al. Effect of breast feeding on responses of systemic interferon and virus-specific lymphocyte transformation in infants with respiratory syncytial virus infection. J. Med. Virol. 21, 7–14 (1987).

    CAS  PubMed  Google Scholar 

  38. 38

    Friss, H. E., Rubin, L. G., Carsons, S., Baranowski, J. & Lipsitz, P. J. Plasma fibronectin concentrations in breast fed and formula fed neonates. Arch. Dis. Child. 63, 528–532 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Stephens, S., Kennedy, C. R., Lakhani, P. K. & Brenner, M. K. In vivo immune responses of breast- and bottle-fed infants to tetanus toxoid antigen and to normal gut flora. Acta Paediatr. Scand. 73, 426–432 (1984).

    CAS  PubMed  Google Scholar 

  40. 40

    Prentice, A. et al. The nutritional role of breast-milk IgA and lactoferrin. Acta Paediatr. Scand. 76, 592–598 (1987).

    CAS  PubMed  Google Scholar 

  41. 41

    Lucas, A. & Cole, T. J. Breast milk and neonatal necrotising enterocolitis. Lancet 336, 1519–1523 (1990).

    CAS  PubMed  Google Scholar 

  42. 42

    World Health Organization/United Nations Children's Fund. Innocenti Declaration on the Protection, Promotion and Support of Breastfeeding. UNICEF [online], http://www.unicef.org/programme/breastfeeding/innocenti.htm (1990).

  43. 43

    Huffman, S., Yeager, B., Levine, R., Shelton, J. & Labbok, M. Breastfeeding Saves Lives: An Estimate of the Impact of Breastfeeding on Infant Mortality in Developing Countries. (NURTURE, Washington DC, 1991).

  44. 44

    Cushing, A. H. et al. Breastfeeding reduces risk of respiratory illness in infants. Am. J. Epidemiol. 147, 863–870 (1998).

    CAS  PubMed  Google Scholar 

  45. 45

    Perera, B. J., Ganesan, S., Jayarasa, J. & Ranaweera, S. The impact of breastfeeding practices on respiratory and diarrhoeal disease in infancy: a study from Sri Lanka. J. Trop. Pediatr. 45, 115–118 (1999).

    CAS  PubMed  Google Scholar 

  46. 46

    Clemens, J. et al. Early initiation of breastfeeding and the risk of infant diarrhea in rural Egypt. Pediatrics [online], 104, e3 (1999).

    CAS  PubMed  Google Scholar 

  47. 47

    Kramer, M. S. et al. Promotion of breastfeeding intervention trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA 285, 413–420 (2001).

    CAS  PubMed  Google Scholar 

  48. 48

    Butz, W. P., Habicht, J. P. & DaVanzo, J. Environmental factors in the relationship between breastfeeding and infant mortality: the role of sanitation and water in Malaysia. Am. J. Epidemiol. 119, 516–525 (1984).

    CAS  PubMed  Google Scholar 

  49. 49

    Arifeen, S. et al. Exclusive breastfeeding reduces acute respiratory infection and diarrhea deaths among infants in Dhaka slums. Pediatrics [online], 108, e67 (2001).

    CAS  PubMed  Google Scholar 

  50. 50

    WHO Collaborative Study Team on the Role of Breastfeeding on the Prevention of Infant Mortality. Effect of breastfeeding on infant and child mortality due to infectious diseases in less developed countries: a pooled analysis. Lancet 355, 451–455 (2000).

  51. 51

    Pelletier, D. & Frongillo, E. Changes in child survival are strongly associated with changes in malnutrition in developing countries. J. Nutr. 133, 107–119 (2003).

    CAS  PubMed  Google Scholar 

  52. 52

    Piwoz, E. G., Creed de Kanashiro, H., Lopez de Romana, G. L., Black, R. E. & Brown, K. H. Feeding practices and growth among low-income Peruvian infants: a comparison of internationally-recommended definitions. Int. J. Epidemiol. 25, 103–114 (1996).

    CAS  PubMed  Google Scholar 

  53. 53

    Villalpando, S. & Lopez-Alarcon, M. Growth faltering is prevented by breastfeeding in underprivileged infants in Mexico City. J. Nutr. 130, 546–552 (2000).

    CAS  PubMed  Google Scholar 

  54. 54

    Froozani, M. D., Permehzadeh, K., Motlagh, A. R. & Golestan, B. Effect of breastfeeding education on the feeding pattern and health of infants in their first 4 months in the Islamic Republic of Iran. Bull. World Health Organ. 77, 381–385 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. 55

    Arifeen, S. E., Black, R. E., Caulfield, L. E., Antelman, G. & Baqui, A. H. Determinants of infant growth in the slums of Dhaka: size and maturity at birth, breastfeeding and morbidity. Eur. J. Clin. Nutr. 55, 167–178 (2001).

    CAS  PubMed  Google Scholar 

  56. 56

    Kramer, M. S. et al. Breastfeeding and infant growth: biology or bias? Pediatrics 110, 343–347 (2002).

    PubMed  Google Scholar 

  57. 57

    Anderson, J. W., Johnstone, B. M. & Remley, D. T. Breast-feeding and cognitive development: a meta-analysis. Am. J. Clin. Nutr. 70, 525–535 (1999).

    CAS  PubMed  Google Scholar 

  58. 58

    Ball, T. M. & Bennett, D. M. The economic impact of breastfeeding. Pediatr. Clin. North Am. 48, 253–262 (2001).

    CAS  PubMed  Google Scholar 

  59. 59

    Bhatnagar, S., Jain, N. P. & Tiwari, V. K. Cost of infant feeding in exclusive and partially breastfed infants. Indian Pediatr. 33, 655–658 (1996).

    CAS  PubMed  Google Scholar 

  60. 60

    Valdes, V. et al. The impact of a hospital and clinic-based breastfeeding promotion programme in a middle class urban environment. J. Trop. Pediatr. 39, 142–151 (1993).

    CAS  PubMed  Google Scholar 

  61. 61

    World Health Organization. International Code of Marketing of Breast-milk Substitutes. WHO [online], http://www.who.int/nut/documents/code_english.PDF (1981).

  62. 62

    Allain, A. & Chetley, A. Protecting Infant Health. A Health Workers' Guide to the International Code of Marketing of Breastmilk Substitutes 10th edn (International Baby-Food Action Network/International Child Development Centre, Penang, 2002).

    Google Scholar 

  63. 63

    United Nations. Resolution adopted by the General Assembly. United Nations Millennium Declaration. UN A/RES/55/2. UNICEF [online], http://www.un.org/millennium/declaration/ares552e.pdf (2000).

  64. 64

    United Nations. Resolution adopted by the General Assembly. A World Fit for Children. UN A/RES/S-27/2, article 37.5. UNICEF [online], http://www.unicef.org/specialsession/docs_new/documents/A-RES-S27-2E.pdf (2002).

  65. 65

    Ross, J. & Labbok, M. Modeling the effects of different infant feeding strategies on young child survival and mother-to-child transmission of HIV. Am. J. Public Health (in the press).

  66. 66

    Becker, S., Rutstein, S. & Labbok, M. H. Estimation of births averted due to breastfeeding and increases in levels of contraception needed to substitute for breastfeeding. J. Biosoc. Sci. 35, 559–574 (2003).

    PubMed  Google Scholar 

  67. 67

    World Health Organization, United Nations Children's Fund, Institut Français de Recherche Scientifique pour le Developpement en Cooperation & University of California at Davis. Complementary Feeding of Young Children in Developing Countries: A Review of Current Scientific Knowledge (World Health Organization, Geneva, 1998).

  68. 68

    Richter, J. Holding Corporations Accountable: Corporate Conduct, International Codes, and Citizen Action (Zed, London, 2001).

    Google Scholar 

  69. 69

    Latham, M. & Kisanga, P. Four Country Study of Impact of HIV on Infant Feeding. UNICEF consultants' report. UNICEF [online], http://www.unsystem.org/scn/Publications/AnnualMeeting/SCN28/28breast feeding.htm

  70. 70

    World Health Organization, Joint United Nations (UN) Programme on HIV/AIDS, UN Children's Fund, Food and Agriculture Organization of the UN, UN High Commissioner for Refugees, UN World Food Programme, World Bank, UN Population Fund & International Atomic Energy Agency. HIV and Infant Feeding: Framework for Priority Action (World Health Organization, Geneva, 2003).

  71. 71

    Coutsoudis, A. et al. Morbidity in children born to women infected with human immunodeficiency virus in South Africa: does mode of feeding matter? Acta Paediatr. 92, 890–895 (2003).

    CAS  PubMed  Google Scholar 

  72. 72

    Phadke, M. A. et al. Replacement-fed infants born to HIV-infected mothers in India have a high early postpartum rate of hospitalization. J. Nutr. 133, 3153–3157 (2003).

    CAS  PubMed  Google Scholar 

  73. 73

    Coutsoudis, A. et al. Method of feeding and transmission of HIV-1 from mothers to children by 15 months of age: prospective cohort study from Durban, South Africa. AIDS 15, 379–387 (2001).

    CAS  PubMed  Google Scholar 

  74. 74

    United Nations. Resolution adopted by the General Assembly. Convention on the Rights of the Child. UN A/RES/44/25, annex 44 UN GAOR Supp. No. 49 at 167, UN Doc. A/44/49. UNHCR [online], http://www.unhchr.ch/html/menu3/b/k2crc.htm (1989).

  75. 75

    United Nations Children's Fund. Plan of Action for Implementing the World Declaration on the Survival, Protection and Development of Children in the 1990s (United Nations Children's Fund, New York, 2000).

  76. 76

    Food and Agriculture Organization of the United Nations. World Declaration and Plan of Action for Nutrition. FAO [online], http://www.fao.org/docrep/U9920t/u9920t0a.htm (1992).

  77. 77

    United Nations Population Information Network. Report of the International Conference on Population and Development. UN A/CONF.171/13. UN [online], http://www.un.org/popin/icpd/conference/offeng/poa.html (1994).

  78. 78

    United Nations. Beijing Declaration and Platform for Action. Report of the Fourth World Conference on Women. UN A/CONF.177/20 and A/CONF.177/20/Add.1. UN [online], http://www.un.org/documents/ga/conf177/aconf177-20en.htm, http://www.un.org/documents/ga/conf177/aconf177-20add1en.htm (1995).

  79. 79

    World, Health Organization & United Nations Children's Fund. Global Strategy for Infant and Young Child Feeding (World Health Organization, Geneva, 2003).

  80. 80

    Rutstein, S. O. in DHS Analytical Studies (ORC Macro, Calverton, Maryland, in the press).

  81. 81

    Guthrie, P. Georgia leads nation as syphilis increases. The Atlanta Journal-Constitution (Atlanta) (21 Nov 2003).

    Google Scholar 

  82. 82

    Holroyd, E., Tam, S. M., Marie, L. A. & Li, F. Editorial. Gender Research Centre Newsletter (Apr 2001). Gender Research Centre [online], http://www.cuhk.edu.hk/hkiaps/grc/activity/pub_news.html.

    Google Scholar 

Download references

Acknowledgements

The statements in this publication are the views of the authors and do not necessarily reflect the policies or views of UNICEF or the University of Texas, United States.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Miriam H. Labbok.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez Gene

CCL5

CD4

CD8

CXCL8

erythropoietin

granulocyte colony-stimulating factor

IFN-α

IFN-γ

IL-1β

IL-6

IL-10

IL-12

macrophage colony-stimulating factor

MUC1

TGF-β

TNF

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Labbok, M., Clark, D. & Goldman, A. Breastfeeding: maintaining an irreplaceable immunological resource. Nat Rev Immunol 4, 565–572 (2004). https://doi.org/10.1038/nri1393

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing