The human milk microbiota plays a role in health of the infant

11.15.2012

 

Human milk is a complex biological fluid, which satisfies the nutritional requirements of rapidly growing infants. In a recent study, it has been suggested that human milk microbiota may play a major role in the health of the infants.1 It educates the infant immune system and confers a certain degree of protection against pathogens.2 These effects reflect the synergistic action of many bioactive molecules which are present in colostrum and milk such as: immunocompetent cells, immunoglobulins, fatty acids, polyamines, oligosaccharides, lysozyme, lactoferrin and other glycoproteins and antimicrobial peptides.3 These molecules inactivate pathogens individually, additively, and synergistically.4 Many studies have recently suggested that colostrum and breast milk are continuous sources of probiotic bacteria to the infant gut.5-12

Many bacterial species and bacterial DNA sequencies have been isolated from human milk. There is predominance of staphylococci, streptococci, lactic acid bacteria (LAB), propionibacteria and closely related Gram-positive bacteria in human milk.5,6,13,14 Human milk has also been shown to be a source of live bifidobacteria in the infant’s gut.12    These microbes have now been found to be secreted by the mammary gland and are not considered contamination,  but nature’s way of colonizing the babies gut with the proper bacteria.1

The mammary microbiota (see above) are transient in nature.  Its development starts during the last trimester of pregnancy, reaches the highest complexity at the end of last trimester, remains constant throughout lactation, then declines sharply at weaning and rapidly disappears when there is no milk in the mammary gland.

It has been suggested that exposure of the breastfed infant to such a number of bacterial species may exert beneficial effects against diarrheal and respiratory diseases and may reduce the risk of other diseases, such as diabetes or obesity.15,16

Bacteria in human milk may play several roles in the infant gut. They can contribute to the reduction, incidence and severity of infections in the breastfed infant by different mechanisms, such as production of antimicrobial compounds,7,10,11,17  Such bacteria may improve the intestinal barrier function by increasing mucine production and reduce intestinal permeability.17 Recently, the administration of a human milk Lactobacillus strain in infants during 6 months led to 46%, 27%, and 30% reductions in the incidence of gastrointestinal infections, upper respiratory tract infections, and total number of infections, respectively.18

Bacteria in milk may also participate in the promoting maturation of the infant immune system, as some strains may modulate both natural and acquired immune responses in humans.19,20,21 These bacteria enhance macrophage production of cytokines in the absence of an inflammatory stimulus and behave as potent activators of NK cells, moderate activators of CD4+ and CD8+ T cells and regulatory T cells which play important role in immune responses. Human milk bacteria also have a remarkable potential to play metabolic roles in the infant. Some lactobacilli and bifidobacteria may help to create a specific “healthy” microbiota in the infant gut.22,23 These microorganisms might also contribute to infant digestion through the breakdown of sugars and proteins.

Lactobacilli strains are metabolically active in the infant gut and increase the production of functional metabolites such as butyrate, which is the main energy source for intestinal cells and also modulates intestinal function. As a result, they improve the intestinal habitat of infants by increasing fecal moisture, stool frequency and volume.24,25

 

Thus, human milk is a source of bacteria to the infant gut, where they may play a variety of anti-infectious, immunomodulatory, and metabolic roles.

 

Sonia Shoukat  M.D.

Thomas W. Hale Ph.D.

InfantRisk Center

 

References:

1) Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM. The human milk microbiota: Origin and potential roles in health and disease. Pharmacol Res. 2012 Sep 10. pii: S1043-6618(12)00165-X. doi: 10.1016/j.phrs.2012.09.001.

2) Morrow AL, Rangel JM. Human milk protection against infectious diarrhea: implications for prevention and clinical care. Seminars in Pediatric Infectious Diseases 2004;15:221–8.

3) Newburg DS. Innate immunity and human milk. Journal of Nutrition 2005;135:1308–12.

4) Isaacs CE. Human milk inactivates pathogens individually, additively and syn-ergistically. Journal of Nutrition 2005;135:1286–8.

5) Martín R, Langa S, Reviriego C, Jiménez E, Marín ML, Xaus J, et al. Human milk is a source of lactic acid bacteria for the infant gut. Journal of Pediatrics 2003;143:754–8.

6) Heikkilä MP, Saris PEJ. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. Journal of Applied Microbiology 2003;95:471–8.

7) Beasley SS, Saris PEJ. Nisin-producing Lactococcus lactis strains isolated from human milk. Applied and Environment Microbiology 2004;70:5051–3.

8) Jiménez E, Delgado S, Maldonado A, Arroyo R, Albújar M, García N, et al. Staphylococcus epidermidis: a differential trait of the fecal.

9) Jiménez E, Fernández L, Delgado S, García N, Albújar M, Gómez A, et al. Assessment of the bacterial diversity of human colostrum by cultural-based techniques. Analysis of the staphylococcal and enterococcal populations. Research in Microbiology 2008;159:595–601.

10) Martín R, Olivares M, Marín ML, Fernández L, Xaus J, Rodríguez JM. Probiotic potential of 3 lactobacilli strains isolated from breast milk. Journal of Human Lactation 2005;21:8–17.

 11) Martín R, Jiménez E, Olivares M, Marín ML, Fernández L, Xaus J, et al. Lacto-bacillus salivarius CECT 5713, a potential probiotic strain isolated from infant feces and breast milk of a mother–child pair. International Journal of Food Microbiology 2006;112:35–43.

12) Martín R, Jiménez E, Heilig HG, Fernández L, Marín ML, Zoetendal EG, et al. Isolation of bifidobacteria from breast milk and assessment of the bifi-dobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Applied and Environment Microbiology 2009;75: 965–9.

13) Gavin A, Ostovar K. Microbiological characterization of human milk. Journal of Food Protection 1977;40:614–6.

14)  West PA, Hewitt JH, Murphy OM. The influence of methods of collection and storage on the bacteriology of human milk. Journal of Applied Bacteriology 1979;46:269–77.

15) Hunt KM, Foster JA, Forney LJ, Schütte UME, Beck DL, Abdo Z, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 2011;6:e21313.

16] Sanz Y. Gut microbiota and probiotics in maternal and infant health. American Journal of Clinical Nutrition 2011;94(Suppl 6):2000S–5S.

17) Olivares M, Díaz-Ropero MP, Martín R, Rodríguez JM, Xaus J. Antimicrobial potential of four Lactobacillus strains isolated from breast milk. Journal of Applied Microbiology 2006;101:72–9.

18) Maldonado J, Ca˜nabate F, Sempere L, Vela F, Sánchez AR, Narbona E, et al. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. Journal of Pediatric Gastroenterology and Nutrition 2012;54(January (1)):55–61.

19) Diaz-Ropero MP, Martin R, Sierra S, Lara-Villoslada F, Rodríguez JM, Xaus J, et al. Two Lactobacillus strains, isolated from breast milk, differently mod-ulate the immune response. Journal of Applied Microbiology 2006;102: 337–43.

20) Olivares M, Díaz-Ropero MP, Gómez N, Lara-Villoslada F, Sierra S, Maldonado JA, et al. The consumption of two new probiotic strains, Lactobacillus gasseri CECT5714 and Lactobacillus coryniformis CECT5711, boost the immune system of healthy adults. International Microbiology 2006;9:47–52.

21) Olivares M, Díaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonollá J, Navas M, et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 2007;23:254–60.

22) Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, et al. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. Journal of Biological Chemistry 2011;286:34583–92.

23) Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America 2011;108(Suppl 1):4653–8.

24) Kirjavainen PV, Apostolou E, Arvola T, Salminen SJ, Gibson GR, Isolauri E. Characterizing the composition of intestinal microflora as a prospective treatment target in infant allergic disease. FEMS Immunology and Medical Microbiology 2001;32:1–7.

25) Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, et al. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. Journal of Biological Chemistry 2011;286:34583–92.