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Impacts of Prebiotic-Supplemented Diets and Breastmilk on Population and Diversity of Lactobacilli Established in Thai Healthy Infants

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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

  1. 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

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. Walter J (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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

    Article  Google Scholar 

  13. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. Boehm G, Moro G (2008) Structural and functional aspects of prebiotics used in infant nutrition. J Nutr 138:1818–1828

    Article  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    Article  CAS  PubMed  Google Scholar 

  22. 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

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. Kimura K, Nishio T, Mizoguchi C, Koizumi A (2010) Analysis of the composition of Lactobacilli in humans. Biosci Microflora 29:47–50

    Article  CAS  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. Heikkila MP, Saris PEJ (2003) Inhibition of Staphylococcus aureus by the commensal bacteria of human milk. J Appl Microbiol 95:471–478

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  PubMed  PubMed Central  Google Scholar 

  32. 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

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. 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

    Article  PubMed  PubMed Central  Google Scholar 

  35. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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

    Article  PubMed  PubMed Central  Google Scholar 

  37. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. Boehm G, Fanaro S, Jelinek J, Stah B, Marini A (2003) Prebiotic concept for infant nutrition. Acta Paediatr Suppl 91:64–67

    CAS  PubMed  Google Scholar 

  41. Salminen S, Isolauri E (2006) Intestinal colonization, microbiota and probiotics. J Pediatr 149:115–120

    Article  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. Kaplan H, Hutkins RW (2000) Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Appl Environ Microbiol 66:2682–2684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

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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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Correspondence to 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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