Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health

Nutrition Reviews

Volumn 73, Issue 7, 2015, Pages 426-437

  Jost, Ted ^a   Lacroix, Christophe ^a   Braegger, Christian ^b   Chassard, Christophe ^a  

^a Institute of Food   (Switzerland)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

Enteromammary pathway; Gut health; Human milk bacteria; Human milk oligosaccharides; Microbiota; Neonate

Indexed keywords

OLIGOSACCHARIDE;

ACTINOBACTERIA; ARTICLE; BACTERIUM CONTAMINATION; BACTEROIDES; BACTEROIDETES; BIFIDOBACTERIUM; BREAST MILK; COMMENSAL; ENTEROCOCCUS; FIRMICUTES; HUMAN; INTESTINE FLORA; LACTOBACILLUS; NEWBORN; NONHUMAN; PHASE 4 CLINICAL TRIAL; PROPIONIBACTERIUM; PROTEOBACTERIA; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS SALIVARIUS; BACTERIUM; CHEMISTRY; CLASSIFICATION; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; INFANT; MICROBIOLOGY;

BACTERIA; BACTEROIDES; BIFIDOBACTERIUM; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; INFANT; LACTOBACILLUS; MILK, HUMAN; OLIGOSACCHARIDES;

EID: 84949186367     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1093/nutrit/nuu016     Document Type: Article

References (131)

1. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A. 1998;95:6578-6583.
2. Backhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science. 2005;307:1915-1920.
3. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003;361: 512-519.
4. Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6:237ra265.
5. Jimenez E, Fernandez L, Marin ML, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005;51:270-274.
6. Maynard CL, Elson CO, Hatton RD, et al. Reciprocal interactions of the intestinal microbiota and immune system. Nature. 2012;489:231-241.
7. Morrow AL, Rangel JM. Human milk protection against infectious diarrhea: implications for prevention and clinical care. Semin Pediatr Infect Dis. 2004;15:221-228.
8. Walker A. Breast milk as the gold standard for protective nutrients. J Pediatr. 2010;156 (Suppl):S3-S7.
9. Hosea Blewett HJ, Cicalo MC, Holland CD, et al. The immunological components of human milk. Adv Food Nutr Res. 2008;54:45-80.
10. Turin CG, Ochoa TJ. The role of maternal breast milk in preventing infantile diarrhea in the developing world. Curr Trop Med Rep. 2014;1:97-105.
11. Bauer J, Gerss J. Longitudinal analysis of macronutrients and minerals in human milk produced by mothers of preterm infants. Clin Nutr. 2011;30:215-220.
12. Isaacs CE. Human milk inactivates pathogens individually, additively, and synergistically. J Nutr. 2005;135:1286-1288.
13. Wagner CL, Taylor SN, Johnson D. Host factors in amniotic fluid and breast milk that contribute to gut maturation. Clin Rev Allergy Immunol. 2008;34:191-204.
14. Drozdowski LA, Clandinin T, Thomson AB. Ontogeny, growth and development of the small intestine: understanding pediatric gastroenterology. World J Gastroenterol. 2010;16:787-799.
15. Heikkila MP, Saris PE. Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol. 2003;95:471-478.
16. Gavin A, Ostovar K. Microbiological characterization of human milk. J Food Protect. 1977;40:614-616.
17. West PA, Hewitt JH, Murphy OM. Influence of methods of collection and storage on the bacteriology of human-milk. J Applied Bacteriol. 1979;46:269-277.
18. Martin R, Langa S, Reviriego C, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr. 2003;143:754-758.
19. Martin V, Maldonado-Barragan A, Moles L, et al. Sharing of bacterial strains between breast milk and infant feces. J Hum Lact. 2012;28:36-44.
20. Martin R, Jimenez E, Heilig H, et al. Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol. 2009; 75:965-969.
21. Perez PF, Dore J, Leclerc M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics 2007;119:e724-e732.
22. Jimenez E, Delgado S, Fernandez L, et al. Assessment of the bacterial diversity of human colostrum and screening of staphylococcal and enterococcal populations for potential virulence factors. Res Microbiol. 2008;159:595-601.
23. Jimenez E, Delgado S, Maldonado A, et al. Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol. 2008; 8:doi:10.1186/1471-2180-8-143.
24. Solis G, de Los Reyes-Gavilan CG, Fernandez N, et al. Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe. 2010;16:307-310.
25. Albesharat R, Ehrmann MA, Korakli M, et al. Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst Appl Microbiol. 2011;34:148-155.
26. Jara S, Sanchez M, Vera R, et al. The inhibitory activity of Lactobacillus spp. isolated from breast milk on gastrointestinal pathogenic bacteria of nosocomial origin. Anaerobe. 2011;17:474-477.
27. Jost T, Lacroix C, Braegger CP, et al. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2013;16:2891-2904.
28. Jost T, Lacroix C, Braegger C, et al. Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr. 2013;110:1253-1262.
29. Bode L. Human milk oligosaccharides: prebiotics and beyond. Nutr Rev. 2009;67 (Suppl 2):S183-S191.
30. Beasley SS, Saris PE. Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol. 2004;70:5051-5053.
31. Novak FR, Almeida JA, Silva GO, et al. Human colostrum: a natural source of probiotics?. J Pediatr (Rio J). 2001;77:265-270.
32. Khodayar-Pardo P, Mira-Pascual L, Collado MC, et al. Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J Perinatol. 2014;34:599-605.
33. Hunt KM, Foster JA, Forney LJ, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One. 2011;6:e21313.
34. Alp G, Aslim B. Relationship between the resistance to bile salts and low pH with exopolysaccharide (EPS) production of Bifidobacterium spp. isolated from infants feces and breast milk. Anaerobe. 2010;16:101-105.
35. Collado MC, Delgado S, Maldonado A, et al. Assessment of the bacterial diversity of breast milk of healthy women by quantitative real-time PCR. Lett Appl Microbiol. 2009;48:523-528.
36. Gronlund MM, Gueimonde M, Laitinen K, et al. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin Exp Allergy. 2007;37: 1764-1772.
37. Gueimonde M, Laitinen K, Salminen S, et al. Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatology. 2007;92:64-66.
38. Cabrera-Rubio R, Collado MC, Laitinen K, et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr. 2012;96:544-551.
39. Sinkiewicz G, Nordstrom EA. Occurrence of Lactobacillus reuteri, lactobacilli and bifidobacteria in human breast milk. Pediatr Res. 2005;58:doi:10.1203/00006450-200508000-00382.
40. Makino H, Kushiro A, Ishikawa E, et al. Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism. Appl Environ Microbiol. 2011;77:6788-6793.
41. Martin R, Heilig GH, Zoetendal EG, et al. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J Appl Microbiol. 2007;103:2638-2644.
42. Jimenez E, Fernandez L, Maldonado A, et al. Oral administration of Lactobacillus strains isolated from breast milk as an alternative for the treatment of infectious mastitis during lactation. Appl Environ Microbiol. 2008;74:4650-4655.
43. Soto A, Martin V, Jimenez E, et al. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr. 2014;59:78-88.
44. Collado MC, Laitinen K, Salminen S, et al. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res. 2012;72:77-85.
45. Qutaishat SS, Stemper ME, Spencer SK, et al. Transmission of Salmonella enterica serotype typhimurium DT104 to infants through mother's breast milk. Pediatrics. 2003;111:1442-1446.
46. Martin R, Heilig HGHJ, Zoetendal EG, et al. Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res Microbiol. 2007;158:31-37.
47. Delgado S, Arroyo R, Jimenez E, et al. Staphylococcus epidermidis strains isolated from breast milk of women suffering infectious mastitis: potential virulence traits and resistance to antibiotics. BMC Microbiol. 2009;9:doi:10.1186/1471-2180-9-82.
48. Sinkiewicz G, Ljunggren L. Occurrence of Lactobacillus reuteri in human breast milk. Microb Ecol Health Dis. 2008;20:122-126.
49. Martin R, Jimenez E, Olivares M, et al. Lactobacillus salivarius CECT 5713, a potential probiotic strain isolated from infant feces and breast milk of a mother-child pair. Int J Food Microbiol. 2006;112:35-43.
50. Jeurink PV, van Bergenhenegouwen J, Jimenez E, et al. Human milk: a source of more life than we imagine. Benef Microbes. 2013;4:17-30.
51. Hungate RE. A roll tube method for cultivation of strict anaerobes. In: JR Norris, DW Ribbons, eds. Methods in Microbiology, Vol. 3, Part B. New York: Academic Press; 1969:117-132.
52. Lagier JC, Armougom F, Million M, et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect. 2012;18:1185-1193.
53. Soejima T, Minami J, Yaeshima T, et al. An advanced PCR method for the specific detection of viable total coliform bacteria in pasteurized milk. Appl Microbiol Biotechnol. 2012;95:485-497.
54. Martín R, Langa S, Reviriego C, et al. The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics. Trends Food Sci Technol. 2004;15:121-127.
55. Jost T, Lacroix C, Braegger CP, et al. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One. 2012;7:e44595.
56. Abrahamsson TR, Sinkiewicz G, Jakobsson T, et al. Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr. 2009;49:349-354.
57. Arboleya S, Ruas-Madiedo P, Margolles A, et al. Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breastmilk. Int J Food Microbiol. 2010;149:28-36.
58. Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe. 2011;17:478-482.
59. Bisgaard H, Li N, Bonnelykke K, et al. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol. 2011;128:646-652.
60. Ismail IH, Oppedisano F, Joseph SJ, et al. Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants. Pediatric Allergy Immunol. 2012;23:674-681.
61. Wang M, Karlsson C, Olsson C, et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol. 2008;121: 129-134.
62. FAO/WHO. Report of a Joint FAO/WHO Working Group on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada; 2002.
63. Maldonado-Barragan A, Caballero-Guerrero B, Jimenez E, et al. Enterocin C, a class IIb bacteriocin produced by E. faecalis C901, a strain isolated from human colostrum. Int J Food Microbiol. 2009;133:105-112.
64. Mehanna NSH, Tawfik NF, Salem MME, et al. Assessment of potential probiotic bacteria isolated from breast milk. MEJSR 2013;14:354-360.
65. Jimenez E, Villar-Tajadura MA, Marin M, et al. Complete genome sequence of Bifidobacterium breve CECT 7263, a strain isolated from human milk. J Bacteriol. 2012;194:3762-3763.
66. Olivares M, Diaz-Ropero MP, Martin R, et al. Antimicrobial potential of four Lactobacillus strains isolated from breast milk. J Appl Microbiol. 2006;101: 72-79.
67. Diaz-Ropero MP, Martin R, Sierra S, et al. Two Lactobacillus strains, isolated from breast milk, differently modulate the immune response. J Appl Microbiol. 2007; 102:337-343.
68. Maldonado J, Lara-Villoslada F, Sierra S, et al. Safety and tolerance of the human milk probiotic strain Lactobacillus salivarius CECT5713 in 6-month-old children. Nutrition. 2010;26:1082-1087.
69. Sierra S, Lara-Villoslada F, Sempere L, et al. Intestinal and immunological effects of daily oral administration of Lactobacillus salivarius CECT5713 to healthy adults. Anaerobe. 2010;16:195-200.
70. Langa S, Maldonado-Barragan A, Delgado S, et al. Characterization of Lactobacillus salivarius CECT 5713, a strain isolated from human milk: from genotype to phenotype. Appl Microbiol Biotechnol. 2012;94:1279-1287.
71. Martin R, Olivares M, Marin ML, et al. Probiotic potential of 3 Lactobacilli strains isolated from breast milk. J Hum Lact. 2005;21:8-17.
72. Mane J, Loren V, Pedrosa E, et al. Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflamm Bowel Dis. 2009;15:1155-1163.
73. Maldonado J, Canabate F, Sempere L, et al. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J Pediatr Gastroenterol Nutr. 2012;54:55-61.
74. Martin V, Maldonado-Barragan A, Jimenez E, et al. Complete genome sequence of Streptococcus salivarius PS4, a strain isolated from human milk. J Bacteriol. 2012;194:4466-4467.
75. Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol. 2004;70:5810-5817.
76. Vernia P, Caprilli R, Latella G, et al. Fecal lactate and ulcerative colitis. Gastroenterology. 1988;95:1564-1568.
77. Chassard C, de Wouters T, Lacroix C. Probiotics tailored to the infant: a window of opportunity. Curr Opin Biotechnol. 2014;26:141-147.
78. Palanduz A, Palanduz S, Guler K, et al. Brucellosis in a mother and her young infant: probable transmission by breast milk. Intern J Infect Dis. 2000;4:55-56.
79. Bolin CA, Koellner P. Human-to-human transmission of Leptospira interrogans by milk. J Infect Dis. 1988;158:246-247.
80. Svabic-Vlahovic M, Pantic D, Pavicic M, et al. Transmission of Listeria monocytogenes from mother's milk to her baby and to puppies. Lancet. 1988; 332:doi:10.1016/S0140-6736(88)90276-0.
81. Le Thomas I, Mariani-Kurkdjian P, Collignon A, et al. Breast milk transmission of a Panton-Valentine leukocidin-producing Staphylococcus aureus strain causing infantile pneumonia. J Clin Microbiol. 2001;39:728-729.
82. Novak FR, Da Silva AV, Hagler AN, et al. Contamination of expressed human breast milk with an epidemic multiresistant Staphylococcus aureus clone. J Med Microbiol. 2000;49:1109-1117.
83. Kawada M, Okuzumi K, Hitomi S, et al. Transmission of Staphylococcus aureus between healthy, lactating mothers and their infants by breastfeeding. J Hum Lact. 2003;19:411-417.
84. Bingen E, Denamur E, Lambert-Zechovsky N, et al. Analysis of DNA restriction fragment length polymorphism extends the evidence for breast milk transmission in Streptococcus agalactiae late-onset neonatal infection. J Infect Dis. 1992; 165:569-573.
85. Olver WJ, Bond DW, Boswell TC, et al. Neonatal group B streptococcal disease associated with infected breast milk. Arch Dis Child Fetal Neonatal Ed. 2000;83: F48-F49.
86. Ramsay DT, Mitoulas LR, Kent JC, et al. The use of ultrasound to characterize milk ejection in women using an electric breast pump. J Hum Lact. 2005;21: 421-428.
87. Ramsay DT, Kent JC, Owens RA, et al. Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics. 2004;113:361-367.
88. Kong HH, Segre JA. Skin microbiome: looking back to move forward. J Invest Dermatol. 2012;132:933-939.
89. Bik EM, Long CD, Armitage GC, et al. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 2010;4:962-974.
90. Martin DH, Zozaya M, Lillis R, et al. The microbiota of the human genitourinary tract: trying to see the forest through the trees. Trans Am Clinical and Climatol Assoc. 2012;123:242-256.
91. Rescigno M, Urbano M, Valzasina B, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol. 2001;2:361-367.
92. Arroyo R, Martin V, Maldonado A, et al. Treatment of infectious mastitis during lactation: antibiotics versus oral administration of Lactobacilli isolated from breast milk. Clin Infect Dis. 2010;50:1551-1558.
93. Urashima T, Taufik E, Fukuda K, et al. Recent advances in studies on milk oligosaccharides of cows and other domestic farm animals. Biosci Biotechnol Biochem. 2013;77:455-466.
94. Urashima T, Asakuma S, Leo F, et al. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv Nutr. 2012;3:473S-482S.
95. Coppa GV, Pierani P, Zampini L, et al. Lactose, oligosaccharide and monosaccharide content of milk from mothers delivering preterm newborns over the first month of lactation. Minerva Pediatr. 1997;49:471-475.
96. Gabrielli O, Zampini L, Galeazzi T, et al. Preterm milk oligosaccharides during the first month of lactation. Pediatrics. 2011;128:e1520-e1531.
97. Coppa GV, Gabrielli O, Pierani P, et al. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics. 1993;91:637-641.
98. Chaturvedi P, Warren CD, Altaye M, et al. Fucosylated human milk oligosaccharides vary between individuals and over the course of lactation. Glycobiology. 2001;11:365-372.
99. Coppa GV, Pierani P, Zampini L, et al. Oligosaccharides in human milk during different phases of lactation. Acta Paediatr Suppl. 1999;88:89-94.
100. Erney RM, Malone WT, Skelding MB, et al. Variability of human milk neutral oligosaccharides in a diverse population. J Pediatr Gastroenterol Nutr. 2000;30: 181-192.
101. Ninonuevo MR, Lebrilla CB. Mass spectrometric methods for analysis of oligosaccharides in human milk. Nutr Rev. 2009;67 (Suppl 2):S216-S226.
102. Aldredge DL, Geronimo MR, Hua S, et al. Annotation and structural elucidation of bovine milk oligosaccharides and determination of novel fucosylated structures. Glycobiology. 2013;23:664-676.
103. Ninonuevo MR, Park Y, Yin H, et al. A strategy for annotating the human milk glycome. J Agric Food Chem. 2006;54:7471-7480.
104. LoCascio RG, Desai P, Sela DA, et al. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl Environ Microbiol. 2010;76:7373-7381.
105. Oozeer R, van Limpt K, Ludwig T, et al. Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides. Am J Clin Nutr. 2013;98:561S-571S.
106. Knol J, Scholtens P, Kafka C, et al. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr. 2005;40:36-42.
107. Marcobal A, Barboza M, Froehlich JW, et al. Consumption of human milk oligosaccharides by gut-relatedmicrobes. J Agric Food Chem. 2010;58:5334-5340.
108. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22:1147-1162.
109. Marcobal A, Sonnenburg JL. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect. 2012;18 (Suppl 4):12-15.
110. Ward RE, Ninonuevo M, Mills DA, et al. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol Nutr Food Res. 2007;51: 1398-1405.
111. Ward RE, Ninonuevo M, Mills DA, et al. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl Environ Microbiol. 2006;72:4497-4499.
112. LoCascio RG, Ninonuevo MR, Freeman SL, et al. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J Agric Food Chem. 2007;55:8914-8919.
113. Rockova S, Rada V, Nevoral J, et al. Inter-species differences in the growth of bifidobacteria cultured on human milk oligosaccharides. Folia Microbiol. 2012;57: 321-324.
114. Chichlowski M, German JB, Lebrilla CB, et al. The influence of milk oligosaccharides on microbiota of infants: opportunities for formulas. Annu Rev Food Sci Technol. 2011;2:331-351.
115. Ruiz-Moyano S, Totten SM, Garrido DA, et al. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol. 2013;79:6040-6049.
116. Asakuma S, Hatakeyama E, Urashima T, et al. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem. 2011;286:34583-34592.
117. Marcobal A, Barboza M, Sonnenburg ED, et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe. 2011;10:507-514.
118. Newburg DS. Oligosaccharides in human milk and bacterial colonization. J Pediatr Gastroenterol Nutr. 2000;30 (Suppl 2):S8-S17.
119. Simon PM, Goode PL, Mobasseri A, et al. Inhibition of Helicobacter pylori binding to gastrointestinal epithelial cells by sialic acid-containing oligosaccharides. Infect Immun. 1997;65:750-757.
120. Ruiz-Palacios GM, Cervantes LE, Ramos P, et al. Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem. 2003;278: 14112-14120.
121. Andersson B, Porras O, Hanson LA, et al. Inhibition of attachment of Streptococcus pneumoniae and Haemophilus influenzae by human milk and receptor oligosaccharides. J Infect Dis. 1986;153:232-237.
122. Cravioto A, Tello A, Villafan H, et al. 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.
123. Mysore JV, Wigginton T, Simon PM, et al. Treatment of Helicobacter pylori infection in rhesus monkeys using a novel antiadhesion compound. Gastroenterology. 1999;117:1316-1325.
124. Leach JL, Garber SA, Marcon AA, et al. In vitro and in vivo effects of soluble, monovalent globotriose on bacterial attachment and colonization. Antimicrob Agents Chemother. 2005;49:3842-3846.
125. Mastretta E, Longo P, Laccisaglia A, et al. Effect of Lactobacillus GG and breastfeeding in the prevention of rotavirus nosocomial infection. J Pediatr Gastroenterol Nutr. 2002;35:527-531.
126. Gianino P, Mastretta E, Longo P, et al. Incidence of nosocomial rotavirus infections, symptomatic and asymptomatic, in breast-fed and non-breast-fed infants. J Hosp Infect. 2002;50:13-17.
127. Haarman M, Knol J. Quantitative real-time PCR assays to identify and quantify fecal Bifidobacterium species in infants receiving a prebiotic infant formula. Appl Environ Microbiol. 2005;71:2318-2324.
128. Weiss GA, Hennet T. The role of milk sialyllactose in intestinal bacterial colonization. Adv Nutr. 2012;3:483S-488S. 129. Kavanaugh DW, O'Callaghan J, Butto LF, et al. Exposure of subsp. to milk oligosaccharides increases adhesion to epithelial cells and induces a substantial transcriptional response. PLoS One. 2013;8:e67224.
129. Kavanaugh DW, O'Callaghan J, Butto LF, et al. Exposure of subsp. to milk oligosaccharides increases adhesion to epithelial cells and induces a substantial transcriptional response. PLoS One. 2013;8:e67224
130. Shoaf K, Mulvey GL, Armstrong GD, et al. Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells. Infect Immun. 2006;74:6920-6928.
131. Glycom A/S, Lyngby, Denmark. http://www.glycom.com/About_us.asp. Accessed December 3, 2013.