The Influence of early infant-feeding practices on the intestinal microbiome and body composition in infants

Nutrition and Metabolic Insights

Volumn 8, Issue , 2015, Pages

  O’Sullivan, Aifric ^a   Farver, Marie ^b   Smilowitz, Jennifer T ^c  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b Sutter Davis Hospital   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Baby friendly hospital initiative; Bifidobacterium; Body composition; Breastfeeding; Formula feeding; Human milk oligosaccharides; Lactation; Microbiome

Indexed keywords

EID: 84995490289     PISSN: None     EISSN: 11786388     Source Type: Journal    
DOI: 10.4137/NMI.S29530     Document Type: Note

References (117)

1. Pediatrics AAO. AAP Reaffirms Breastfeeding Guidelines. Elk Grove Village, IL: Author; 2012. Available at: http://www.aap.org/en-us/about-the-aap/aap-press-room/pages/AAP-Reaffirms-Breastfeeding-Guidelines.aspx
2. Wittman AB, Wall LL. The evolutionary origins of obstructed labor: bipedalism, encephalization, and the human obstetric dilemma. Obstet Gynecol Surv. 2007; 62(11):739-748.
3. Beck KL, Weber D, Phinney BS, et al. Comparative proteomics of human and macaque milk reveals species-specific nutrition during post-natal development. J Proteome Res. 2015;14(5):2143-2157.
4. Dunsworth HM, Warrener AG, Deacon T, et al. Metabolic hypothesis for human altriciality. Proc Natl Acad Sci U S A. 2012;109(38):15212-15216.
5. Karp H. The fourth trimester and the calming reflex: novel ideas for nurturing young infants. Midwifery Today Int Midwife. 2011;102:25-26.
6. Blomquist H, Jonsbo F, Serenius F, et al. Supplementary feeding in the maternity ward shortens the duration of breast feeding. Acta Paediatr. 1994;83(11): 1122-1126.
7. Nommsen-Rivers L. Examining the effects of labor epidural analgesia on newborn breastfeeding behaviors. J Hum Lact. 2003;19(4):438-439.
8. Ransjö-Arvidson AB, Matthiesen AS, Lilja G, et al. Maternal analgesia during labor disturbs newborn behavior: effects on breastfeeding, temperature, and crying. Birth. 2001;28(1):5-12.
9. Murase M, Nommsen-Rivers L, Morrow AL, et al. Predictors of low milk volume among mothers who delivered preterm. J Hum Lact. 2014;30(4):425-435.
10. Dewey KG, Nommsen-Rivers LA, Heinig MJ, et al. Risk factors for suboptimal infant breastfeeding behavior, delayed onset of lactation, and excess neonatal weight loss. Pediatrics. 2003;112(3):607-619.
11. Riordan J, Gill-Hopple K, Angeron J. Indicators of effective breastfeeding and estimates of breast milk intake. J Hum Lact. 2005;21(4):406-412.
12. Lieberman E, O'Donoghue C. Unintended effects of epidural analgesia during labor: a systematic review. Am J Obstet Gynecol. 2002;186(5):S31-S68.
13. Perrine CG, Scanlon KS, Li R, et al. Baby-friendly hospital practices and meeting exclusive breastfeeding intention. Pediatrics. 2012;130(1):54-60.
14. Cloherty M, Alexander J, Holloway I. Supplementing breast-fed babies in the UK to protect their mothers from tiredness or distress. Midwifery. 2004;20(2): 194-204.
15. Organization WH. Global Nutrition Targets 2025: Breastfeeding Policy Brief. 2014.
16. Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host & Microbe. 2015;17(5): 690-703. ISSN 1931-3128, http://dx.doi.org/10.1016/j.chom.2015.04.004.
17. Praveen P, Jordan F, Priami C, et al. The role of breast-feeding in infant immune system: a systems perspective on the intestinal microbiome. Microbiome. 2015; 3(1):1-12.
18. 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(6):478-482.
19. Penders J, Thijs C, Vink C, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511-521.
20. Mitsuoka T, Kaneuchi C. Ecology of the bifidobacteria. Am J Clin Nutr. 1977; 30(11):1799-1810.
21. Le Huërou-Luron I, Blat S, Boudry G. Breast-v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev. 2010; 23(1):23-36.
22. Siigur U, Ormisson A, Tamm A. Faecal short-chain fatty acids in breast-fed and bottle-fed infants. Acta Paediatr. 1993;82(6-7):536-538.
23. Bullen C, Tearle P, Stewart M. The effect of "humanised" milks and supplemented breast feeding on the faecal flora of infants. J Med Microbiol. 1977;10(4):403-413.
24. Penders J, Gerhold K, Stobberingh EE, et al. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol. 2013;132(3):601-607.
25. McGuire S. Centers for disease control and prevention. 2013. strategies to prevent obesity and other chronic diseases: the CDC guide to strategies to support breastfeeding mothers and babies. Atlanta, GA: US Department of Health and Human Services, 2013. Adv Nutr. 2014;5(3):291-292.
26. Ip S, Chung M, Raman G, et al. Breastfeeding and maternal and infant health outcomes in developed countries. Evid Rep Technol Assess (Full Rep). 2007;153: 1-186. Rockville, MD: Agency for Healthcare Research and Quality.
27. Zeitlin J, Mohangoo A, Delnorn M, et al. European perinatal health report. The health and care of pregnant women and babies in Europe in 2010. 2013.
28. Begley C, Gallagher L, Clarke M, et al. The National Infant Feeding Survey 2008/ Prepared for the Health Service Executive by Cecily Begley. University of Dublin, Trinity College Dublin; 2008.
29. Philipp BL, Merewood A, Miller LW, et al. Baby-friendly hospital initiative improves breastfeeding initiation rates in a US hospital setting. Pediatrics. 2001; 108(3):677-681.
30. Centers for Disease Control and Prevention (CDC). Vital signs: hospital practices to support breastfeeding-United States, 2007 and 2009. MMWR Morb Mortal Wkly Rep. 2011;60(30):1020.
31. Semenic S, Loiselle C, Gottlieb L. Predictors of the duration of exclusive breastfeeding among first-time mothers. Res Nurs Health. 2008;31(5):428-441.
32. Organization WH. Unicef. Protecting, Promoting and Supporting Breast-Feeding: The Special Role of Maternity Services. World Health Organization; 1989.
33. Cattaneo A, Buzzetti R. Quality improvement report: effect on rates of breast feeding of training for the baby friendly hospital initiative. BMJ. 2001; 323(7325):1358.
34. Tsai T-I, Huang S-H, Lee S-YD. Maternal and hospital factors associated with first-time mothers' breastfeeding practice: a prospective study. Breastfeed Med. 2015;10(6):334-340.
35. Wagner EA, Chantry CJ, Dewey KG, et al. Breastfeeding concerns at 3 and 7 days postpartum and feeding status at 2 months. Pediatrics. 2013;132(4):e865-e875.
36. Zakarija-Grković I, Šegvić O, Božinović T, et al. Hospital practices and breastfeeding rates before and after the UNICEF/WHO 20-hour course for maternity staff. J Hum Lact. 2012;28(3):389-399.
37. General OotS. The Surgeon General's Call to Action to Support Breastfeeding. Rockville, MD: General OotS; 2011.
38. Al-Sahab B, Lanes A, Feldman M, et al. Prevalence and predictors of 6-month exclusive breastfeeding among Canadian women: a national survey. BMC Pediatr. 2010;10:20.
39. Dieterich CM, Felice JP, O'Sullivan E, et al. Breastfeeding and health outcomes for the mother-infant dyad. Pediatr Clin North Am. 2013;60(1):31-48.
40. Pak-Gorstein S, Haq A, Graham EA. Cultural influences on infant feeding practices. Pediatr Rev. 2009;30(3):e11.
41. Chantry CJ, Dewey KG, Peerson JM, et al. In-hospital formula use increases early breastfeeding cessation among first-time mothers intending to exclusively breastfeed. J Pediatr. 2014;164(6):1339-1345.
42. Chantry CJ, Nommsen-Rivers LA, Peerson JM, et al. Excess weight loss in first-born breastfed newborns relates to maternal intrapartum fluid balance. Pediatrics. 2011;127(1):e171-e179.
43. Noel-Weiss J, Woodend AK, Peterson WE, et al. An observational study of associations among maternal fluids during parturition, neonatal output, and breastfed newborn weight loss. Int Breastfeed J. 2011;6:9.
44. Merry H, Montgomery A. Do breastfed babies whose mothers have had labor epidurals lose more weight in the first 24 hours of life. Acad Breastfeed Med News Views. 2000;6:3.
45. Riordan J, Gross A, Angeron J, et al. The effect of labor pain relief medication on neonatal suckling and breastfeeding duration. J Hum Lact. 2000;16(1):7-12.
46. Volmanen P, Valanne J, Alahuhta S. Breast-feeding problems after epidural analgesia for labour: a retrospective cohort study of pain, obstetrical procedures and breast-feeding practices. Int J Obstet Anesth. 2004;13(1):25-29.
47. Jonas W, Johansson LM, Nissen E, et al. Effects of intrapartum oxytocin administration and epidural analgesia on the concentration of plasma oxytocin and prolactin, in response to suckling during the second day postpartum. Breastfeed Med. 2009;4(2):71-82.
48. Flaherman VJ, Aby J, Burgos AE, et al. Effect of early limited formula on duration and exclusivity of breastfeeding in at-risk infants: an RCT. Pediatrics. 2013; 131(6):1059-1065.
49. Morton J, Hall J, Wong R, et al. Combining hand techniques with electric pumping increases milk production in mothers of preterm infants. J Perinatol. 2009;29(11):757-764.
50. Parker LA, Sullivan S, Krueger C, et al. Effect of early breast milk expression on milk volume and timing of lactogenesis stage II among mothers of very low birth weight infants: a pilot study. J Perinatol. 2012;32(3):205-209.
51. Ohyama M, Watabe H, Hayasaka Y. Manual expression and electric breast pumping in the first 48 h after delivery. Pediatr Int. 2010;52(1):39-43.
52. Gagnon AJ, Leduc G, Waghorn K, et al. In-hospital formula supplementation of healthy breastfeeding newborns. J Hum Lact. 2005;21(4):397-405.
53. Macdonald P, Ross S, Grant L, et al. Neonatal weight loss in breast and formula fed infants. Arch Dis Child Fetal Neonatal Ed. 2003;88(6):F472-F476.
54. Becker GE, Remmington T. Early additional food and fluids for healthy breastfed full-term infants. Cochrane Database Syst Rev. 2014;12:CD006462.
55. Del Chierico F, Vernocchi P, Petrucca A, et al. Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PLoS One. 2015;10(9): e0137347.
56. Moles L, Gomez M, Heilig H, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoS One. 2013;8(6):e66986.
57. Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107(26):11971-11975.
58. 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(19):6788-6793.
59. Schwartz S, Friedberg I, Ivanov IV, et al. A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biol. 2012;13(4):r32.
60. Maga EA, Desai PT, Weimer BC, et al. Consumption of lysozyme-rich milk can alter microbial fecal populations. Appl Environ Microbiol. 2012;78(17): 6153-6160.
61. Oda H, Wakabayashi H, Yamauchi K, et al. Lactoferrin and bifidobacteria. Biometals. 2014;27(5):915-922.
62. Maga EA, Weimer BC, Murray JD. Dissecting the role of milk components on gut microbiota composition. Gut Microbes. 2013;4(2):136-139.
63. Mantis NJ, Rol N, Corthesy B. Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011;4(6):603-611.
64. Ninonuevo MR, Park Y, Yin H, et al. A strategy for annotating the human milk glycome. J Agric Food Chem. 2006;54(20):7471-7480.
65. Niñonuevo MR, Perkins PD, Francis J, et al. Daily variations in oligosaccharides of human milk determined by microfluidic chips and mass spectrometry. J Agric Food Chem. 2007;56(2):618-626.
66. Ninonuevo MR, Ward RE, LoCascio RG, et al. Methods for the quantitation of human milk oligosaccharides in bacterial fermentation by mass spectrometry. Anal Biochem. 2007;361(1):15-23.
67. Sela D, Chapman J, Adeuya A, et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A. 2008;105(48):18964-18969.
68. Sela DA. Bifidobacterial utilization of human milk oligosaccharides. Int J Food Microbiol. 2011;149(1):58-64.
69. Sela DA, Garrido D, Lerno L, et al. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol. 2012;78(3):795-803.
70. Sela DA, Li Y, Lerno L, et al. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem. 2011;286(14):11909.
71. Garrido D, Dallas DC, Mills DA. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology. 2013;159(pt 4):649-664.
72. Garrido D, Kim JH, German JB, et al. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One. 2011;6(3):e17315.
73. 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(19):6040-6049.
74. Garrido D, Barile D, Mills DA. A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv Nutr. 2012;3(3):415S-421S.
75. Garrido D, Nwosu C, Ruiz-Moyano S, et al. Endo-beta-N-acetylglucosaminidases from infant gut-associated bifidobacteria release complex N-glycans from human milk glycoproteins. Mol Cell Proteomics. 2012;11(9):775-785.
76. Garrido D, Ruiz-Moyano S, Jimenez-Espinoza J, et al. Utilization of galactooligosaccharides by Bifidobacterium longum subsp. infantis isolates. Food Microbiol. 2012;33(2):262-270.
77. Garrido D, Ruiz-Moyano S, Mills DA. Release and utilization of N-acetyl-D-glucosamine from human milk oligosaccharides by Bifidobacterium longum subsp. infantis. Anaerobe. 2012;18(4):430-435.
78. Marcobal A, Barboza M, Froehlich JW, et al. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. 2010;58(9): 5334-5340.
79. LoCascio R, Ninonuevo M, Freeman S, 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(22):8914-8919.
80. 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(22):7373-7381.
81. Yoshida E, Sakurama H, Kiyohara M, et al. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology. 2012;22(3):361-368.
82. Kim J-H, An HJ, Garrido D, et al. Proteomic analysis of Bifidobacterium longum subsp. infantis reveals the metabolic insight on consumption of prebiotics and host glycans. PLoS One. 2013;8(2):e57535.
83. Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 2011;6(3):285-306.
84. Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestine important to infants' and children's health? J Pediatr Gastroenterol Nutr. 2015;60(3):294-307.
85. Bernet M-F, Brassart D, Neeser J, et al. Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl Environ Microbiol. 1993;59(12):4121-4128.
86. Chichlowski M, De Lartigue G, German JB, et al. Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. J Pediatr Gastroenterol Nutr. 2012;55(3):321-327.
87. O'Hara AM, O'Regan P, Fanning Á, et al. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology. 2006;118(2):202-215.
88. Ewaschuk JB, Diaz H, Meddings L, et al. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol. 2008; 295(5):G1025-G1034.
89. Ganguli K, Meng D, Rautava S, et al. Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am J Physiol. 2013;304(2):G132-G141.
90. Scully P, MacSharry J, O'Mahony D, et al. Bifidobacterium infantis suppression of Peyer's patch MIP-1α and MIP-1β secretion during Salmonella infection correlates with increased local CD4+CD25+ T cell numbers. Cell Immunol. 2013; 281(2):134-140.
91. Fukuda S, Toh H, Hase K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469(7331):543-547.
92. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341(6145): 569-573.
93. Huda M, Lewis Z, Kalanetra K, et al. Stool microbiota and vaccine responses of infants. Pediatrics. 2014;134:1-11.
94. Underwood MA, Kalanetra KM, Bokulich NA, et al. A comparison of two probiotic strains of bifidobacteria in premature infants. J Pediatr. 2013;163(6): 1585-1591.
95. Underwood MA, German JB, Lebrilla CB, et al. Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut. Pediatr Res. 2014;77(1-2): 229-235.
96. Sakata H, Yoshioka H, Fujita K. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur J Pediatr. 1985;144(2):186-190.
97. Dominguez-Bello MG, Blaser MJ, Ley RE, et al. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology. 2011;140(6):1713-1719.
98. Matsuki T, Watanabe K, Tanaka R, et al. Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers. Appl Environ Microbiol. 1999;65(10):4506-4512.
99. Lewis ZT, Totten SM, Smilowitz JT, et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 2015;3(1):13.
100. Ventura M, Elli M, Reniero R, et al. Molecular microbial analysis of Bifidobacterium isolates from different environments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA). FEMS Microbiol Ecol. 2001; 36(2-3):113-121.
101. Wopereis H, Oozeer R, Knipping K, et al. The first thousand days-intestinal microbiology of early life: establishing a symbiosis. Pediatr Allergy Immunol. 2014;25(5):428-438.
102. Kleessen B, Bunke H, Tovar K, et al. Influence of two infant formulas and human milk on the development of the faecal flora in newborn infants. Acta Paediatr. 1995;84(12):1347-1356.
103. Dewey KG. Growth characteristics of breast-fed compared to formula-fed infants. Biol Neonate. 1998;74(2):94-105.
104. Gale C, Logan KM, Santhakumaran S, et al. Effect of breastfeeding compared with formula feeding on infant body composition: a systematic review and meta-analysis. Am J Clin Nutr. 2012;95(3):656-669.
105. Arenz S, Ruckerl R, Koletzko B, et al. Breast-feeding and childhood obesity[mdash]a systematic review. Int J Obes Relat Metab Disord. 2004;28(10): 1247-1256.
106. Ong KK, Loos RJF. Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr. 2006;95(8):904-908.
107. Lönnerdal B. Infant formula and infant nutrition: bioactive proteins of human milk and implications for composition of infant formulas. Am J Clin Nutr. 2014;99(3): 712S-717S.
108. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013;60(1):49-74.
109. Lonnerdal B. Infant formula and infant nutrition: bioactive proteins of human milk and implications for composition of infant formulas. Am J Clin Nutr. 2014; 99(3):712S-717S.
110. Woo JG, Guerrero ML, Altaye M, et al. Human milk adiponectin is associated with infant growth in two independent cohorts. Breastfeed Med. 2009;4(2): 101-109.
111. Schuster S, Hechler C, Gebauer C, et al. Leptin in maternal serum and breast milk: association with infants' body weight gain in a longitudinal study over 6 months of lactation. Pediatr Res. 2011;70(6):633-637.
112. Li R, Fein SB, Grummer-Strawn LM. Do infants fed from bottles lack self-regulation of milk intake compared with directly breastfed infants? Pediatrics. 2010;125(6):e1386-e1393.
113. Rossiter M, Colapinto C, Khan MA, et al. Breast, formula and combination feeding in relation to childhood obesity in Nova Scotia, Canada. Matern Child Health J. 2015;19(9):2048-2056.
114. Holmes AV, Auinger P, Howard CR. Combination feeding of breast milk and formula: evidence for shorter breast-feeding duration from the national health and nutrition examination survey. J Pediatr. 2011;159(2):186-191.
115. Bogen D, Hanusa B, Whitaker R. The effect of breast-feeding with and without formula use on the risk of obesity at 4 years of age. Obes Res. 2004;12(9): 1527-1535.
116. Gillman MW, Rifas-Shiman SL, Camargo CA Jr, et al. Risk of overweight among adolescents who were breastfed as infants. JAMA. 2001;285(19): 2461-2467.
117. Chivers P, Hands B, Parker H, et al. Body mass index, adiposity rebound and early feeding in a longitudinal cohort (Raine study). Int J Obes. 2010;34(7):1169-1176.