Human breast milk and infant formulas differentially modify the intestinal microbiota in human infants and host physiology in rats

Journal of Nutrition

Volumn 146, Issue 2, 2016, Pages 191-199

  Liu, Zhenmin ^a   Roy, Nicole C ^b,c   Guo, Yanhong ^a   Jia, Hongxin ^a   Ryan, Leigh ^b   Samuelsson, Linda ^b   Thomas, Ancy ^d   Plowman, Jeff ^d   Clerens, Stefan ^d,e   Day, Li ^b   Young, Wayne ^b  

^a State Key Laboratory of Dairy Biotechnology   (China)

^b AGRESEARCH GRASSLANDS   (New Zealand)

^c MASSEY UNIVERSITY   (New Zealand)

^d AGRESEARCH LTD   (New Zealand)

^e UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

Breast milk; Infant formula; Metabolomics; Microbiota; Transcriptomics

Indexed keywords

ACETIC ACID; PROTEOME; SHORT CHAIN FATTY ACID; TRANSCRIPTOME; VOLATILE FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MILK; BIFIDOBACTERIUM; BREAST MILK; CECUM; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; FECES; FECES MICROFLORA; FEMALE; GENE EXPRESSION; HISTOLOGY; HUMAN; HUMAN EXPERIMENT; INFANT; INFANT FEEDING; INTESTINAL TISSUE; INTESTINE FLORA; MALE; METABOLITE; METABOLOMICS; MICROBIAL COMMUNITY; MICROBIAL METABOLISM; NEWBORN; NONHUMAN; NUTRITIONAL VALUE; PHYSIOLOGY; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; RAT; WEANING; ANIMAL; BREAST FEEDING; CHEMISTRY; DIET; GROWTH, DEVELOPMENT AND AGING; INFANT NUTRITION; INTESTINE; METABOLISM; MICROBIOLOGY; MILK; SPRAGUE DAWLEY RAT;

ANIMALS; BIFIDOBACTERIUM; BREAST FEEDING; DIET; FATTY ACIDS, VOLATILE; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INFANT, NEWBORN; INTESTINES; MALE; MILK; MILK, HUMAN; RATS, SPRAGUE-DAWLEY; WEANING;

EID: 84959287341     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.223552     Document Type: Article

References (56)

1. 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;23:23-36.
2. Sjögren YM, Tomicic S, Lundberg A, Bottcher MF, Bjorksten B, Sverremark-Ekstrom E, Jenmalm MC. Influence of early gut microbiota on the maturation of childhood mucosal and systemic immune responses. Clin Exp Allergy 2009;39:1842-51.
3. Rogier EW, Frantz AL, Bruno MEC, Wedlund L, Cohen DA, Stromberg AJ, Kaetzel CS. Secretory antibodies in breast milk promote long-term intestinal homeostasis by regulating the gut microbiota and host gene expression. Proc Natl Acad Sci 2014;111:3074-9.
4. Bergström A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, Molgaard C, Michaelsen KF, Licht TR. Establishment of intestinal microbiota during early life: A longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 2014;80:2889-900.
5. Sela DA, Li Y, Lerno L, Wu S, Marcobal AM, German JB, Chen X, Lebrilla CB, Mills DA. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem 2011;286: 11909-18.
6. Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J Nutr 2005;135:1304-7.
7. Iyengar SR, Walker WA. Immune factors in breast milk and the development of atopic disease. J Pediatr Gastroenterol Nutr 2012;55: 641-7.
8. Mah KW, Chin VI, Wong WS, Lay C, Tannock GW, Shek LP, Aw MM, Chua KY, Wong HB, Panchalingham A, et al. Effect of a milk formula containing probiotics on the fecal microbiota of Asian infants at risk of atopic diseases. Pediatr Res 2007;62:674-9.
9. Wang M, Karlsson C, Olsson C, Adlerberth I, Wold AE, Strachan DP, Martricardi PM, Aberg N, Perkin MR, Tripodi S, et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol 2008;121:129-34.
10. Kalliomäki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr 2008;87:534-8.
11. Reeves PG, Nielsen FH, Fahey GC, Jr. AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993;123:1939-51.
12. Young W, Roy NC, Lee J, Lawley B, Otter D, Henderson G, McCann MJ, Tannock GW. Changes in bowel microbiota induced by feeding resistant starch stimulate transcriptomic and physiological responses in the weanling host. Appl Environ Microbiol 2012;78: 6656-64.
13. Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O, et al. Colonization-induced host-gut microbial metabolic interaction. MBio 2011;2:e00271-e10.
14. Young W, Hine BC, Wallace OAM, Callaghan M, Bibiloni R. Transfer of intestinal bacterial components to mammary secretions in the cow. PeerJ 2015;3:e888.
15. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-6.
16. Knoch B, Barnett MP, McNabb WC, Zhu S, Park ZA, Khan A, Roy NC. Dietary arachidonic acid-mediated effects on colon inflammation using transcriptome analysis. Mol Nutr Food Res 2010;54 Suppl 1:S62-74.
17. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004;5:R80.
18. Smyth GK: Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
19. Jiang Z, Gentleman R. Extensions to gene set enrichment. Bioinformatics 2007;23:306-13.
20. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 2005;102: 15545-50.
21. Matthews L, Gopinath G, Gillespie M, Caudy M, Croft D, de Bono B, Garapati P, Hemish J, Hermjakob H, Jassal B, et al. Reactome knowledgebase of human biological pathways and processes. Nucleic Acids Res 2009;37:D619-22.
22. Young W, Roy NC, Lee J, Lawley B, Otter D, Henderson G, Tannock GW. Bowel microbiota moderate host physiological responses to dietary konjac in weanling rats. J Nutr 2013;143:1052-60.
23. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 2006;78:779-87.
24. Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam B, Hau DD, Psychogios N, Dong E, Bouatra S, et al. HMDB: A knowledgebase for the human metabolome. Nucleic Acids Res 2009;37:D603-10.
25. Smith CA, O'Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, Custodio DE, Abagyan R, Siuzdak G. METLIN: A metabolite mass spectral database. Ther Drug Monit 2005;27:747-51.
26. LêCao KA, Gonzalez I, Dejean S. integrOmics: An R package to unravel relationships between two omics datasets. Bioinformatics 2009; 25:2855-6.
27. R Core Team. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2010.
28. Wu D, Lim E, Vaillant F, Asselin-Labat ML, Visvader JE, Smyth GK. ROAST: Rotation gene set tests for complex microarray experiments. Bioinformatics 2010;26:2176-82.
29. Koletzko B, Baker S, Cleghorn G, Neto UF, Gopalan S, Hernell O, Hock QS, Jirapinyo P, Lonnerdal B, Pencharz P, et al. Global standard for the composition of infant formula: Recommendations of an ESPGHAN coordinated international expert group. J Pediatr Gastroenterol Nutr 2005;41:584-99.
30. Siigur U, Ormisson A, Tamm A. Faecal short-chain fatty acids in breastfed and bottle-fed infants. Acta Paediatr 1993;82:536-8.
31. Mountzouris KC, McCartney AL, Gibson GR. Intestinal microflora of human infants and current trends for its nutritional modulation. Br J Nutr 2002;87:405-20.
32. Kripke SA, Fox AD, Berman JM, Settle RG, Rombeau JL. Stimulation of intestinal mucosal growth with intracolonic infusion of short-chain fatty acids. JPEN J Parenter Enteral Nutr 1989;13:109-16.
33. Zaibi MS, Stocker CJ, O'Dowd J, Davies A, Bellahcene M, Cawthorne MA, Brown AJ, Smith DM, Arch JR. Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett 2010;584:2381-6.
34. Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, Terasawa K, Kashihara D, Hirano K, Tani T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun 2013;4:1829.
35. Bode L. Human milk oligosaccharides: Every baby needs a sugar mama. Glycobiology 2012;22:1147-62.
36. Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G, Stokholm J, Smith B, Krogfelt KA: 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 e641-645.
37. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC: Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012, 129:434-440, 440 e431-432.
38. Azad MB, Konya T, Guttman DS, Field CJ, Sears MR, HayGlass KT, Mandhane PJ, Turvey SE, Subbarao P, Becker AB, et al: Infant gut microbiota and food sensitization: Associations in the first year of life. Clin Exp Allergy 2015;45:632-43.
39. Bassett SA, Young W, Barnett MP, Cookson AL, McNabb WC, Roy NC. Changes in composition of caecal microbiota associated with increased colon inflammation in interleukin-10 gene-deficient mice inoculated with Enterococcus species. Nutrients 2015;7:1798-816.
40. Lapthorne S, Pereira-Fantini PM, Fouhy F, Wilson G, Thomas SL, Dellios NL, Scurr M, O'Sullivan O, Ross RP, Stanton C, et al. Gut microbial diversity is reduced and is associated with colonic inflammation in a piglet model of short bowel syndrome. Gut Microbes 2013;4:212-21.
41. Maharshak N, Packey CD, Ellermann M, Manick S, Siddle JP, Huh EY, Plevy S, Sartor RB, Carroll IM. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes 2013;4:316-24.
42. Jiang W, Wu N, Wang X, Chi Y, Zhang Y, Qiu X, Hu Y, Li J, Liu Y. Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease. Sci Rep 2015;5:8096.
43. Chinda D, Nakaji S, Fukuda S, Sakamoto J, Shimoyama T, Nakamura T, Fujisawa T, Terada A, Sugawara K. The fermentation of different dietary fibers is associated with fecal clostridia levels in men. J Nutr 2004; 134:1881-6.
44. KalmokoffM, Zwicker B, O'Hara M, Matias F, Green J, Shastri P, Green-Johnson J, Brooks SPJ. Temporal change in the gut community of rats fed high amylose cornstarch is driven by endogenous urea rather than strictly on carbohydrate availability. J Appl Microbiol 2013;114:1516-28.
45. van der Post S, Subramani DB, Backstrom M, Johansson ME, Vester-Christensen MB, Mandel U, Bennett EP, Clausen H, Dahlen G, Sroka A, et al. Site-specific O-glycosylation on the MUC2 mucin protein inhibits cleavage by the Porphyromonas gingivalis secreted cysteine protease (RgpB). J Biol Chem 2013;288:14636-46.
46. Robertson BR, O'Rourke JL, Neilan BA, Vandamme P, On SL, Fox JG, Lee A. Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. Int J Syst Evol Microbiol 2005;55:1199-204.
47. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334: 105-8.
48. Kelder T, Stroeve JHM, Bijlsma S, Radonjic M, Roeselers G. Correlation network analysis reveals relationships between diet-induced changes in human gut microbiota and metabolic health. Nutr Diabetes 2014;4: e122.
49. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 2010;107:14691-6.
50. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci 2009;106:2365-70.
51. Maathuis AJ, van den Heuvel EG, Schoterman MH, Venema K. Galacto-oligosaccharides have prebiotic activity in a dynamic in vitro colon model using a (13)C-labeling technique. J Nutr 2012;142: 1205-12.
52. Boehm G, Stahl B. Oligosaccharides from milk. J Nutr 2007;137: 847S-9S.
53. Corazziari ES. Intestinal mucus barrier in normal and inflamed colon. J Pediatr Gastroenterol Nutr 2009;48 Suppl 2:S54-5.
54. Ricciotti E, FitzGerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol 2011;31:986-1000.
55. Finetti F, Solito R, Morbidelli L, Giachetti A, Ziche M, Donnini S. Prostaglandin E2 regulates angiogenesis via activation of fibroblast growth factor receptor-1. J Biol Chem 2008;283:2139-46.
56. Maceyka M, Payne SG, Milstien S, Spiegel S. Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 2002;1585: 193-201.