Abstract
The relative abundance and diversity of lactobacilli present in feces of infants fed with breastmilk and fructooligosaccharide-galactooligosaccharide (FOS-GOS)-, and inulin-galactooligosaccharide (inulin-GOS)-supplemented infant formulae and combination of both were compared. Fecal lactobacilli rapidly colonized and reached maximum total cell counts, which were significantly higher in the infants fed by combining breastmilk with a formula containing either FOS-GOS (C1-A infant) or inulin-GOS (C2-C infant) and the exclusively formula fed ones (F1-F and F2-H infants) than those detected in the exclusively breast-fed (B1-D and B2-E infants) (P < 0.05). The greatest relative abundance of fecal lactobacilli species was observed in all infant receiving prebiotic-containing diets, whereas bifidobacteria appeared predominantly in exclusively breast-fed infants. The species composition of lactobacilli was highly unique among individual and more variable in both groups of infants receiving breastmilk than the exclusively formula-fed infants. Breastmilk seem to be a great source of indigenous lactobacilli vertically transferred and continuously seeded infants’ gut. Meanwhile, prebiotic supplementation in infant formulae enhanced and sustained the successful colonization of lactobacilli.
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References
Houghteling PD, Walker WA (2015) Why is initial bacterial colonization of the intestine important to infants’ and childrean’s health? J Pediatr Gastroenterol Nutr 60:294–307
Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904
Fan W, Huo G, Li X, Yang L, Duan C, Wang T, Chen J (2013) Diversity of the intestinal microiota in different patterns of feeding infants by lllumina high throughput sequencing. World J Microbiol Biotechnol 26:2365–2372
Heeney DD, Gareau MG, Marco ML (2018) Intestinal Lactobacillus in health and disease, a driver or just along for the ride? Curr Opin Biotechnol 49:140–147
Turpin W, Humblot C, Thomas M, Guyot JP (2010) Lactobacilli as multifaceted probiotics with poorly disclosed molecular mechanisms. Int J Food Microbiol 143:87–102
Walter J (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996
Gomez-Llorente C, Plaza-Diaz J, Aguilera M, Muñoz-Quezada S, Bermudez-Brito M, Peso-Echarri P, Martinez-Silla R, Vasallo-Morillas MI, Campaña-Martin L, Vives-Piñera I, Ballesta-Martinez MJ, Gil A (2013) Three main factors define changes in fecal microbiota associated with feeding modality in infants. J Pediatr Gastroenterol Nutr 57:461–466
Tanaka M, Nakayama J (2017) Development of the gut microbiota in infancy and its impact on health in later life. Allergol Int 66:515–522
Voreades N, Kozil A, Weir LT (2014) Diet and the development of the human intestinal microbiome. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00494
Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere MF (2013) Development of intestinal microbiota in infants and its impact on health. Trends Microbiol 21:167–173
Wang M, Li M, Wu S, Lebrilla CB, Chapkin RS, Ivanov I, Donovan SM (2015) Fecal microbiota composition of breast-fed infants is correlated with human milk oligosaccharides consumed. J Pediatr Gastroenterol Nutr 60:825–833
Yang B, Chen Y, Stanton C, Ross RP, Lee YK, Zhao J, Zhang H, Chen W (2019) Bifidobacterium and Lactobacillus composition at species level and gut microbiota diversity in infants before 6 weeks. Int J Mol. https://doi.org/10.3390/ijms20133306
Bergstrom A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, Molgaard C, Michaelsen KF, Licht TR (2014) Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 80:2889–2900
Magne F, Hachelaf W, Suau A, Boudraa G, Mangin I, Touhami M, Bouziane-Nedjadi K, Pochart P (2000) A longitudinal study of infant faecal microbiota during weaning. FEMS Microbiol Ecol 58:563–571
Kanjan P, Hongpattarakere T (2016) Antibacterial metabolites secreted under glucose-limited environment of the mimicked proximal colon model by lactobacilli abundant in infant feces. Appl Microbiol Biotechnol 100:7651–7664
Boehm G, Moro G (2008) Structural and functional aspects of prebiotics used in infant nutrition. J Nutr 138:1818–1828
Solis G, de los Reyes-Gavilan CG, Fernandez N, Margolles A, Guemonde M (2010) Establishment and development of lactic acid bacteria and bifidobacteria microbiota in breast-milk and the infant gut. Anaerobe 16:307–310
Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, Stobberingh EE (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521
Hongpattarakere T, Cherntong N, Wichienchot S, Kolida S (2012) In vitro prebiotic evaluation of exopolysaccharide produced by marine isolated lactic acid bacteria. Carbohydr Polym 87:846–852
Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP (2001) Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 6:2578–2585
Uraipan S, Brigidi P, Hongpattarakere T (2014) Antagonistic mechanism of synbiosis between Lactobacillus plantarum CIF17AN2 and green banana starch in the proximal colon model challenged with Salmonella Typhimurium. Anaerobe 28:44–53
Davis EC, Wang M, Donovan SMZ (2017) The role of early life nutrition in the establishment of gastrointestinal microbial composition and function. Gut microbes 8:143–171
Haarman M, Knol J (2006) Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol 72:2359–2365
Kleessen B, Bunke H, Tovar K, Noack J, Sawatzki G (1995) Influence of two infant formulas and human milk on the development of the faecal flora in newborn infants. Acta Paediatr 84:1347–1356
Ahrne S, Lonnermark E, Wold AE, Aberg N, Hesselmar B, Saalman R, Strannegard IL, Molin G, Adlerberth I (2005) Lactobacilli in the intestinal microbiota of Swedish infants. Microbes Infect 7:1256–1262
Kimura K, Nishio T, Mizoguchi C, Koizumi A (2010) Analysis of the composition of Lactobacilli in humans. Biosci Microflora 29:47–50
Soto A, Martin V, Jimenez E, Mader I, Rodriguez MJ, Fernandez L (2014) Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr 59:78–88
Jost T, Lacroix C, Braegger C, Chassard C (2015) Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr Rev 73:426–437
Martin R, Langa S, Reviriego C, Jimenez E, Marin ML, Xaus J, Fernandez L, Rodriguez JM (2003) Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr 143:754–758
Heikkila MP, Saris PEJ (2003) Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 95:471–478
Rodriguez MJ (2014) The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation? Adv Nutr 5:779–784
Kunz C, Rudloff S, Baier W, Klein N, Strobel S (2000) Oligosaccharides in human milk: structural, function, and metabolic aspects. Annu Rev Nutr 20:699–722
Thongaram T, Hoeflinger JL, Chow J, Miller JM (2017) Human milk oligosaccharide consumption by probiotic and human-associated bifidobacteria and lactobacilli. J Dairy Sci 100:7825–7833
Zuniga M, Monedero V, Yebra MJ (2018) Utilization of host-derived glycans by intestinal Lactobacillus and Bifidobacterium species. Front Microbiol. https://doi.org/10.3389/fmicb.2018.01917
Yu ZT, Chen C, Newurg DS (2013) Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 23:1281–1292
Bidart GN, Rodríguez-Díaz J, Pérez-Martínez G, Yebra MJ (2018) The lactose operon from Lactobacillus casei is involved in the transport and metabolism of the human milk oligosaccharide core-2 N-acetyllactosamine. Sci Rep. https://doi.org/10.1038/s41598-018-25660-w
Salvini F, Riva E, Salvatici E, Boehm G, Jelinek J, Banderali G, Giovannini M (2011) A specific prebiotic mixture added to starting infant formula has long-lasting bifidogenic effects. J Nutr 141:1335–1339
Ivakhnenko OS, Nyankovskyy SL (2013) Effect of the specific infant formula mixture of oligosaccharides on local immunity and development of allergic and infectious disease in young children: randomized study. Pediatr Pol 88:398–404
Boehm G, Lidestri M, Casetta P, Jelinek J, Negretti F, Stahl B, Marini A (2002) Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants. Arch Dis Child Fetal Neonat Ed 86:178–181
Boehm G, Fanaro S, Jelinek J, Stah B, Marini A (2003) Prebiotic concept for infant nutrition. Acta Paediatr Suppl 91:64–67
Salminen S, Isolauri E (2006) Intestinal colonization, microbiota and probiotics. J Pediatr 149:115–120
Bakker-Zierikzee AM, Alles MS, Knol J, Kok FJ, Tolboom JJM, Bindels JG (2005) Effects of infant formula containing a mixture of galacto- and fructooligosaccharides or viable Bifidobacterium animalis on the intestinal microflora during the first 4 months of life. Br J Nutr 947:783–790
Schwab C, Ganzle M (2011) Lactic acid bacteria fermentation of human milk oligosaccharide components, human milk oligosaccharides and galactooligosaccharides. FEMS Microbiol Lett 315:141–148
Endo H, Tamura HK, Fukasawa T, Kanegae M, Koga J (2012) Comparison of fructooligosaccharide utilization by Lactobacillus and Bacteroides species. Biosci Biotechnol Biochem 76:176–179
Kaplan H, Hutkins RW (2000) Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Appl Environ Microbiol 66:2682–2684
Takemura N, Hagio M, Ishizuka S, Ito H, Morita T (2010) Inulin prolongs survival of intragastrically administered Lactobacillus plantarum No. 14 in the gut of mice fed a high-fat diet. J Nutr 140:1963–1969
Kanjan P, Hongpattarakere T (2017) Prebiotic efficacy and mechanism of inulin combined with inulin-degrading Lactobacillus paracasei I321 in competition with Salmonella. Carbohydr Polym 69:236–244
Gomez-Gallego C, Garcia-Mantrana I, Salmine S, Collado MC (2016) The human milk microbiome and factors influencing its composition and activity. Semin Fetal Neonat Med 21:400–405
Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96:544–551
Acknowledgements
This research was financially supported by Graduate School, Prince of Songkla University, and the Office of the Higher Education Commission under the CHE-PhD Scholarship program (Grant No. 03–2553) granted to Khanitta Kongnum under supervision of Associate Prof. Tipparat Hongpattarakere.
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This research protocol was reviewed and approved by the Ethics Committee, Faculty of Medicine, Prince of Songkla University (EC Number: 55–244-19–2-3) and (EC Number: 55–243-19–2-3). Verbal informed consent was obtained from all infants’ parents on behalf of the participating baby. The verbal consent was granted by the Ethics Committee because this research presented negligible risks to the infant participants. Moreover, all samples and data were processed and analyzed anonymously.
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Kongnum, K., Taweerodjanakarn, S. & Hongpattarakere, T. Impacts of Prebiotic-Supplemented Diets and Breastmilk on Population and Diversity of Lactobacilli Established in Thai Healthy Infants. Curr Microbiol 77, 1191–1202 (2020). https://doi.org/10.1007/s00284-020-01920-9
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DOI: https://doi.org/10.1007/s00284-020-01920-9