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Breastfeeding: a key modulator of gut microbiota characteristics in late infancy

  • M. Matsuyama (a1), L. F. Gomez-Arango (a2), N. M. Fukuma (a3), M. Morrison (a4) (a5), P. S. W. Davies (a1) and R. J. Hill (a1)...

Abstract

The objective of this study was to investigate the impact of the most commonly cited factors that may have influenced infants’ gut microbiota profiles at one year of age: mode of delivery, breastfeeding duration and antibiotic exposure. Barcoded V3/V4 amplicons of bacterial 16S-rRNA gene were prepared from the stool samples of 52 healthy 1-year-old Australian children and sequenced using the Illumina MiSeq platform. Following the quality checks, the data were processed using the Quantitative Insights Into Microbial Ecology pipeline and analysed using the Calypso package for microbiome data analysis. The stool microbiota profiles of children still breastfed were significantly different from that of children weaned earlier (P<0.05), independent of the age of solid food introduction. Among children still breastfed, Veillonella spp. abundance was higher. Children no longer breastfed possessed a more ‘mature’ microbiota, with notable increases of Firmicutes. The microbiota profiles of the children could not be differentiated by delivery mode or antibiotic exposure. Further analysis based on children’s feeding patterns found children who were breastfed alongside solid food had significantly different microbiota profiles compared to that of children who were receiving both breastmilk and formula milk alongside solid food. This study provided evidence that breastfeeding continues to influence gut microbial community even at late infancy when these children are also consuming table foods. At this age, any impacts from mode of delivery or antibiotic exposure did not appear to be discernible imprints on the microbial community profiles of these healthy children.

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Corresponding author

Address for correspondence: M. Matsuyama, Children’s Nutrition Research Centre, UQ Child Health Research Centre, Faculty of Medicine, The University of Queensland, 62 Graham Street, South Brisbane, QLD 4101, Australia. E-mail: m.matsuyama@uq.edu.au

References

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1. Wopereis, H, Oozeer, R, Knipping, K, Belzer, C, Knol, J. The first thousand days – intestinal microbiology of early life: establishing a symbiosis. Pediatr Allergy Immunol. 2014; 25, 428438.
2. Cusick, SE, Georgieff, MK. The role of nutrition in brain development: the golden opportunity of the “first 1000 days”. J Pediatr. 2016; 175, 1621.
3. Garcia-Mantrana, I, Collado, MC. Obesity and overweight: impact on maternal and milk microbiome and their role for infant health and nutrition. Mol Nutr Food Res. 2016; 60, 18651875.
4. Ma, J, Prince, AL, Bader, D, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun. 2014; 5, 3889.
5. Macpherson, AJ, de Aguero, MG, Ganal-Vonarburg, SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017; 17, 508517.
6. Madan, JC, Hoen, AG, Lundgren, SN, et al. Association of cesarean delivery and formula supplementation with the intestinal microbiome of 6-week-old infants. Jama Pediatr. 2016; 170, 212219.
7. Jakobsson, HE, Abrahamsson, TR, Jenmalm, MC, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014; 63, 559566.
8. 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 USA. 2010; 107, 1197111975.
9. 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, 690703.
10. Bokulich, NA, Chung, J, Battaglia, T, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016; 8, 343ra382.
11. Yassour, M, Vatanen, T, Siljander, H, et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med. 2016; 8, 343ra381.
12. Trasande, L, Blustein, J, Liu, M, et al. Infant antibiotic exposures and early-life body mass. Int J Obesity. 2013; 37, 1623.
13. Bailey, LC, Forrest, CB, Zhang, P, et al. Association of antibiotics in infancy with early childhood obesity. Jama Pediatr. 2014; 168, 10631069.
14. Ajslev, TA, Andersen, CS, Gamborg, M, Sorensen, TI, Jess, T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obesity. 2011; 35, 522529.
15. Azad, MB, Konya, T, Maughan, H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can Med Assoc J. 2013; 185, 385394.
16. Fan, W, Huo, G, Li, X, et al. Diversity of the intestinal microbiota in different patterns of feeding infants by Illumina high-throughput sequencing. World J Microbiol Biotechnol. 2013; 29, 23652372.
17. Roger, LC, McCartney, AL. Longitudinal investigation of the faecal microbiota of healthy full-term infants using fluorescence in situ hybridization and denaturing gradient gel electrophoresis. Microbiology. 2010; 156(Pt 11), 33173328.
18. Fallani, M, Amarri, S, Uusijarvi, A, et al. Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres. Microbiology. 2011; 157(Pt 5), 13851392.
19. Koenig, JE, Spor, A, Scalfone, N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011; 108 Suppl 1(Supplement 1), 45784585.
20. Agans, R, Rigsbee, L, Kenche, H, et al. Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol. 2011; 77, 404412.
21. Yu, Z, Morrison, M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. BioTechniques. 2004; 36, 808812.
22. Klindworth, A, Pruesse, E, Schweer, T, et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013; 41, e1.
23. Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7, 335336.
24. Edgar, RC, Flyvbjerg, H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics. 2015; 31, 34763482.
25. Caporaso, JG, Bittinger, K, Bushman, FD, et al. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010; 26, 266267.
26. DeSantis, TZ, Hugenholtz, P, Larsen, N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006; 72, 50695072.
27. Zakrzewski, M, Proietti, C, Ellis, JJ, et al. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics. 2017; 33, 782783.
28. 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, 58105817.
29. Flint, HJ, Duncan, SH, Scott, KP, Louis, P. Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc. 2015; 74, 1322.
30. Pham, VT, Lacroix, C, Braegger, CP, Chassard, C. Early colonization of functional groups of microbes in the infant gut. Environ Microbiol. 2016; 18, 22462258.
31. Brown, A, Lee, M. Breastfeeding during the first year promotes satiety responsiveness in children aged 18–24 months. Pediatr Obes. 2012; 7, 382390.
32. Arora, T, Sharma, R, Frost, G. Propionate. Anti-obesity and satiety enhancing factor? Appetite. 2011; 56, 511515.
33. Lin, HV, Frassetto, A, Kowalik, EJ Jr., et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One. 2012; 7, e35240.
34. Gomez-Arango, LF, Barrett, HL, McIntyre, HD, et al. Contributions of the maternal oral and gut microbiome to placental microbial colonization in overweight and obese pregnant women. Sci Rep. 2017; 7, 2860.
35. Hasegawa, K, Linnemann, RW, Mansbach, JM, et al. The fecal microbiota profile and bronchiolitis in infants. Pediatrics. 2016; 138, e20160218.
36. Arrieta, MC, Stiemsma, LT, Dimitriu, PA, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015; 7, 307ra152.
37. Thompson, AL, Monteagudo-Mera, A, Cadenas, MB, Lampl, ML, Azcarate-Peril, MA. Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome. Front Cell Infect Microbiol. 2015; 5, 3.
38. Harmsen, HJM, Wildeboer-Veloo, ACM, Raangs, GC, et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr. 2000; 30, 6167.
39. Jost, T, Lacroix, C, Braegger, C, Chassard, C. Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr. 2013; 110, 12531262.
40. Garrido, D, Dallas, DC, Mills, DA. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology. 2013; 159(Pt 4), 649664.
41. Di Gioia, D, Aloisio, I, Mazzola, G, Biavati, B. Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol. 2014; 98, 563.
42. Bakker-Zierikzee, AM, Alles, MS, Knol, J, et al. Effects of infant formula containing a mixture of galacto- and fructo-oligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. Br J Nutr. 2005; 94, 783790.
43. 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, 23182324.
44. Scholtens, PA, Alles, MS, Bindels, JG, et al. Bifidogenic effects of solid weaning foods with added prebiotic oligosaccharides: a randomised controlled clinical trial. J Pediatr Gastroenterol Nutr. 2006; 42, 553559.
45. 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, 507514.
46. Nylund, L, Satokari, R, Salminen, S, de Vos, WM. Intestinal microbiota during early life – impact on health and disease. Proc Nutr Soc. 2014; 73, 457469.
47. Palmer, C, Bik, EM, DiGiulio, DB, Relman, DA, Brown, PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5, e177.
48. Scholtens, PA, Oozeer, R, Martin, R, Amor, KB, Knol, J. The early settlers: intestinal microbiology in early life. Annu Rev Food Sci Technol. 2012; 3, 425447.
49. Huse, SM, Ye, Y, Zhou, Y, Fodor, AA. A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One. 2012; 7, e34242.
50. Konikoff, T, Gophna, U. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol. 2016; 24, 523524.
51. Rutayisire, E, Huang, K, Liu, Y, Tao, F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016; 16, 86.
52. Lim, MY, You, HJ, Yoon, HS, et al. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut. 2017; 66: 1031–1038.
53. Carmody Rachel, N, Gerber Georg, K, Luevano Jr Jesus, M, et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015; 17, 7284.
54. Ussar, S, Griffin, NW, Bezy, O, et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metabolism. 2015; 22, 516530.
55. Garcia-Villalba, R, Gimenez-Bastida, JA, Garcia-Conesa, MT, et al. Alternative method for gas chromatography-mass spectrometry analysis of short-chain fatty acids in faecal samples. J Sep Sci. 2012; 35, 19061913.
56. Bergstrom, A, Skov, TH, Bahl, MI, et al. Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol. 2014; 80, 28892900.

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