Effects of short-chain fructooligosaccharides on faecal bifidobacteria and specific immune response in formula-fed term infants: A randomized, double-blind, placebo-controlled trial

Journal of Nutritional Science and Vitaminology

Volumn 60, Issue 3, 2014, Pages 167-175

  Paineau, Damien ^a   Respondek, Frédérique ^b   Menet, Vincent ^c   Sauvage, Roland ^d   Bornet, Francis ^a,e   Wagner, Anne ^b  

^a Nutri Health SA   (France)

^b Tereos Syral Zone Industrielle et Portuaire ^*  (France)

^c Polyclinique du Bois   (France)

^d Clinique Sainte Marie et Maternité Catholique   (France)

^e AVICENNE HOSPITAL   (France)

Author keywords

Infant formula; Microbiota; Prebiotic

Indexed keywords

CARBOHYDRATE DIET; FAT INTAKE; FRUCTOSE OLIGOSACCHARIDE; IMMUNOGLOBULIN A; OLIGOSACCHARIDE; POLIOMYELITIS VACCINE; PROTEIN INTAKE; VIRUS ANTIBODY;

ADMINISTRATION AND DOSAGE; ARTIFICIAL MILK; BIFIDOBACTERIUM; CALORIC INTAKE; CARBOHYDRATE DIET; CHEMISTRY; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOUBLE BLIND PROCEDURE; FAT INTAKE; FECES; FEMALE; FOLLOW UP; HUMAN; INFANT NUTRITION; MALE; MICROBIOLOGY; NEWBORN; PROTEIN INTAKE; RANDOMIZED CONTROLLED TRIAL;

ANTIBODIES, VIRAL; BIFIDOBACTERIUM; DIETARY CARBOHYDRATES; DIETARY FATS; DIETARY PROTEINS; DOUBLE-BLIND METHOD; ENERGY INTAKE; FECES; FEMALE; FOLLOW-UP STUDIES; FOOD, FORTIFIED; HUMANS; IMMUNOGLOBULIN A; INFANT FORMULA; INFANT NUTRITIONAL PHYSIOLOGICAL PHENOMENA; INFANT, NEWBORN; MALE; OLIGOSACCHARIDES; POLIOVIRUS VACCINES;

EID: 84905173875     PISSN: 03014800     EISSN: 18817742     Source Type: Journal    
DOI: 10.3177/jnsv.60.167     Document Type: Article

References (45)

1. Boehm G, Stahl B. 2007. Oligosaccharides from Milk. J Nutr 137: 847S-849S.
2. Harmsen HJM, Wildeboer-Veloo CM, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30: 61-67.
3. Fallani M, Young D, Scott J, Norin E, Amarri S, Adam R, Aguilera M, Khanna S, Gil A, Edwards CA, Doré J. 2010. Intestinal microbiota of 6-week infants across Europe: Geographic influence beyond delivery mode breastfeeding, and antibiotics. J Pediatr Gastroenterol Nutr 51: 77-84.
4. Kunz C, Rudloff S. 2008. Potential anti-inflammatory and anti-infectious effects of human milk oligosaccharides. Adv Exp Med Biol 606: 455-465.
5. Kuntz S, Rudloff S, Kunz C. 2008. Oligosaccharides from human milk influence growth-related characteristics of intestinally transformed and non-transformed intestinal cells. Br J Nutr 99: 462-471.
6. Stepans MB, Wilhelm SL, Hertzog M, Rodehorst TK, Blaney S, Clemens B, Polak JJ, Newburg DS. 2006. Early consumption of human milk oligosaccharides is inversely related to subsequent risk of respiratory and enteric disease in infants. Breastfeed Med 1: 207-215.
7. Veereman G. 2007. Pediatric applications of inulin and oligofructose. J Nutr 137: 2585-2589.
8. Boehm G, Stahl B, Jelinek J, Knol J, Miniello V, Moro GE. 2005. Prebiotic carbohydrates in human milk and formulas. Acta Paediatr Suppl 94: 18-21.
9. Moro GE, Mosca F, Miniello V, Fanaro S, Jelinek J, Stahl B, Boehm G. 2003. Effects of a new mixture of prebiotics on faecal flora and stools in term infants. Acta Paediatr Suppl 91: 77-79.
10. Moro G, Minoli I, Mosca M, Fanaro S, Jelinek J, Stahl B, Boehm G. 2002. Dosage-related bifidogenic effects of galacto-and fructooligosaccharides in formula-fed term infants. J Pediatr Gastroenterol Nutr 34: 291-295.
11. Roberfroid MB, Gibson GR, Hoyles L, McCartney AL, Rastall RA, Rowland IR, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco MJ, Leotoing L, Witrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A. 2010. Prebiotic effects: metabolic and health benefits. Br J Nutr 104 (Suppl 2): S1-63.
12. Gibson GR, Probert H, van Loo J, Rastall RA, Roberfroid MB. 2004. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17: 259-275.
13. Bouhnik Y, Raskine L, Simoneau G, Paineau D, Bornet F. 2006. The capacity of short-chain fructo-oligosaccharides to stimulate fecal bifidobacteria: A dose-response relationship study in healthy humans. Nutr J 5: 8.
14. Paineau D, Payen F, Panserieu S, Coulombier G, Sobaszek A, Lartigau I, Brabet M, Galmiche JP, Tripodi D, Sacher-Huvelin S, Chapalain V, Zourabichvili O, Respondek F, Wagner A, Bornet FR. 2008. The effects of regular consumption of short-chain fructo-oligosaccharides on digestive comfort of subjects with minor functional bowel disorders. Br J Nutr 99: 311-318.
15. Juffrie M. 2002. Fructooligosaccharide and diarrhea. Biosci Microflora 21: 31-34.
16. Nakamura S, Sarker SA, Wahed MA, Wagatsuma Y, Oku T, Moji K. 2006. Prebiotic effect of daily fructooligosaccharide intake on weight gain and reduction of acute diarrhea among children in a Blangladesh urban slum: a randomized double-masked placebo-controlled study. Tropical Med Health 34: 125-131.
17. Albers R, Antoine J-M, Bourdet-Sicard R, Calder PC, Gleeson M, Lesourd B, Samartin S, Sanderson IR, van Loo J, vas Dias FW, Watzl B. 2005. Markers to measure immunomodulation in human nutrition intervention studies. Br J Nutr 94: 452-481.
18. Haarman M, Knol J. 2005. Quantitative real-time PCR assays to identify and quantify fecal Bifidobacterium species in infants receiving a prebiotic infant formula. Appl Environ Microbiol 71: 2318-2324.
19. 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.
20. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. 2005. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by realtime PCR. FEMS Microbiol Lett 243: 141-147.
21. Fu CJ, Carter JN, Li Y, Porter JH, Kerley MS. 2006. Comparison of agar plate and real-time PCR on enumeration of Lactobacillus, Clostridium perfringens and total anaerobic bacteria in dog faeces. Lett Appl Microbiol 42: 490-494.
22. Malinen E, Rinttila T, Kajander K, Matto J, Kassinen A, Krogius L, Saarela M, Korpela R, Palva A. 2005. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 100: 373-382.
23. Ostrom KM, Cordle CT, Schaller JP, Winship TR, Thomas DJ, Jacobs JR, Blatter MM, Cho S, Gooch WMR, Granoff DM, Faden H, Pickering LK. 2002. Immune status of infants fed soy-based formulas with or without added nucleotides for 1 year: part 1: vaccine responses, and morbidity. J Pediatr Gastroenterol Nutr 34: 137-144.
24. Schmelzle H, Wirth S, Skopnik H, Radke M, Knol J, Bockler H, Bronstrup A, Wells J, Fusch C. 2003. Randomized double-blind study of the nutritional efficacy and bifidogenicity of a new infant formula containing partially hydrolyzed protein, a high b-palmitic acid level and nondigestible oligosaccharides. J Pediatr Gastroenterol Nutr 36: 343-351.
25. Scholtens P, Alles MS, Bindels JG, van der Linde EGM, Tolboom JJM, Knol J. 2006. Bifidogenic effects of solid weaning foods with added prebiotic oligosaccharides: a randomised controlled clinical trial. J Pediatr Gastroenterol Nutr 42: 553-559.
26. WHO. 2006. WHO Child Growth Standards: length/ height-for-age, weight-for-age, weight-for-length, weightfor-height and body mass index-for age: methods and development, World Health Organization, Geneva.
27. Ott SJ, Musfeldt M, Timmis KN, Hampe J, Wenderoth DF, Schreiber S. 2004. In vitro alterations of intestinal bacterial microbiota in fecal samples during storage. Diagn Microbiol Infect Dis 50: 237-245.
28. Rochet V, Rigottier-Gois L, Rabot S, Doré J. 2004. Validation of fluorescent in situ hybridization combined with flow cytometry for assessing interindividual variation in the composition of human fecal microflora during long-term storage of samples. Microbiol Methods 59: 263-270.
29. Rycroft CE, Jones MR, Gibson GR, Rastall RA. 2001. A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol 91: 878-887.
30. 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 Neonatal Ed 86: 178-181.
31. Costalos C, Kapiki A, Apostolou M, Papathoma E. 2008. The effect of a prebiotic supplemented formula on growth and stool microbiology of term infants. Early Hum Dev 84: 45-49.
32. Euler AR, Mitchell DK, Kline R, Pickering LK. 2005. Prebiotic effect of fructooligosaccharides supplemented term infant formula at two concentrations compared with unsupplemented formula and human milk. J Pediatr Gastroenterol Nutr 40: 157-164.
33. Knol J, Scholtens P, Steenbakkers J, Gro S, Helm K, Klarczyk M, Scopfer H, Bockler H, Wells J. 2005. Colon microflora in infants with galacto-and fructooligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr 40: 36-42.
34. Bakker-Zierikee AM, van Tol EAF, Kroes H, Alles MS, Kok FJ, Bindels JG. 2006. Faecal SIgA secretion in infants fed on pre-or probiotic infant formula. Pediatr Allergy Immunol 17: 134-140.
35. Mullie C, Yazourh A, Thibault H, Odou M-F, Singer E, Kalach N, Kremp O, Romond M-B. 2004. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: A randomized, doubleblind, placebo-controlled trial. Pediatr Res 56: 791-795.
36. Cebra JJ. 1999. Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69: 1046S-1051S.
37. Yasui H, Nagaoka N, Mike A, Hayakawa K, Ohwaki M. 1992. Detection of bifidobacterium strains that induce large quantities of IgA. Microbial Ecol Health Dis 5: 155-162.
38. Schley PD, Field CJ. 2002. The immune-enhancing effects of dietary fibres and prebiotics. Br J Nutr 87: S221-S230.
39. Hosono A, Ozawa A, Kato R, Ohnishi Y, Nakaniski Y, Kimura T, Nakamura R. 2003. Dietary fructo-oligosaccharides induce immunoregulation of intestinal IgA secretion by Murine Peyer's patch cells. Biosci Biotechnol Biochem 67: 758-764.
40. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N, Iwase T, Moro I. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mices. Clin Exp Immunol 137: 52-58.
41. Cummings JH, Antoine J-M, Azpiroz F, Bourdet-Sicard R, Brandtzaeg P, Calder PC, Gibson GR, Guarner F, Isolauri E, Pannemans D, Shortt C, Tuijtelaars S, Watzl B. 2004. PASSCLAIM-Gut health and immunity. Eur J Nutr 43: ii118-ii173.
42. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G. 2006. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child 91: 814-819.
43. Arslanoglu S, Moro GE, Boehm G. 2007. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J Nutr 137: 2420-2424.
44. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M. 2007. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: A randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 119: 192-198.
45. Kalliomäki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E. 2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin 107: 129-134.