A randomized placebo-controlled comparison of 2 prebiotic/probiotic combinations in preterm infants: Impact on weight gain, intestinal microbiota, and fecal short-chain fatty acids

Journal of Pediatric Gastroenterology and Nutrition

Volumn 48, Issue 2, 2009, Pages 216-225

  Underwood, Mark A ^a,b   Salzman, Nita H ^c   Bennett, Stephen H ^a   Barman, Melissa ^c   Mills, David A ^b   Marcobal, Angela ^b   Tancredi, Daniel J ^a   Bevins, Charles L ^a   Sherman, Michael P ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Microflora; Prebiotic; Premature infant; Probiotic; Synbiotic

Indexed keywords

CULTURELLE; FRUCTOSE OLIGOSACCHARIDE; PLACEBO; PREBIOTIC AGENT; PROBIOPLUS; PROBIOTIC AGENT; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; IDOLAX; OLIGOSACCHARIDE; VOLATILE FATTY ACID;

ABSENCE OF SIDE EFFECTS; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM DETECTION; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM LONGUM INFANTIS; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG FORMULATION; ENTEROBACTERIACEAE; FECES ANALYSIS; FECES CULTURE; HUMAN; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS RHAMNOSUS; MAJOR CLINICAL STUDY; NEWBORN; PREMATURITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; STAPHYLOCOCCUS; WEIGHT GAIN; BACTERIAL COUNT; BIFIDOBACTERIUM; CHEMISTRY; COMPARATIVE STUDY; FECES; FEMALE; GASTROINTESTINAL TRACT; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LACTOBACILLUS; MALE; MICROBIOLOGY; ORAL DRUG ADMINISTRATION; POLYMERASE CHAIN REACTION; TIME; TREATMENT OUTCOME;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; LACTOBACILLUS; NEGIBACTERIA; STAPHYLOCOCCUS;

ADMINISTRATION, ORAL; BIFIDOBACTERIUM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLONY COUNT, MICROBIAL; FATTY ACIDS, VOLATILE; FECES; FEMALE; GASTROINTESTINAL TRACT; GESTATIONAL AGE; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; LACTOBACILLUS; MALE; OLIGOSACCHARIDES; POLYMERASE CHAIN REACTION; PROBIOTICS; TIME FACTORS; TREATMENT OUTCOME; WEIGHT GAIN;

EID: 66149153878     PISSN: 02772116     EISSN: None     Source Type: Journal    
DOI: 10.1097/MPG.0b013e31818de195     Document Type: Article

References (63)

1. Backhed F, Ley RE, Sonnenburg JL, et al. Host-bacterial mutualism in the human intestine. Science 2005;307:1915-20.
2. Roberts AK. Prospects for further approximation of infant formulas to human milk. Hum Nutr Appl Nutr 1986;40 (Suppl 1):27-37.
3. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999;69:1035S-45S.
4. Sakata H, Yoshioka H, Fujita K. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur J Pediatr 1985;144:186-90.
5. Gewolb IH, Schwalbe RS, Taciak VL, et al. Stool microflora in extremely low birthweight infants. Arch Dis Child Fetal Neonatal Ed 1999;80:F167-73.
6. Millar M, Wilks M, Costeloe K. Probiotics for preterm infants? Arch Dis Child Fetal Neonatal Ed 2003;88:F354-8.
7. Westerbeek EA, van den Berg A, Lafeber HN, et al. The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 2006;25:361-8.
8. Mohan R, Koebnick C, Schildt J, et al. Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: a double-blind, placebo-controlled, randomized study. J Clin Microbiol 2006;44:4025-31.
9. Agarwal R, Sharma N, Chaudhry R, et al. Effects of oral Lactobacillus GG on enteric microflora in low-birth-weight neonates. J Pediatr Gastroenterol Nutr 2003;36:397-402.
10. Vendt N, Grunberg H, Tuure T, et al. Growth during the first 6 months of life in infants using formula enriched with Lactoba-cillus rhamnosus GG: double-blind, randomized trial. J Hum Nutr Diet 2006;19:51-8.
11. Puccio G, Cajozzo C, Meli F, et al. Clinical evaluation of a new starter formula for infants containing live Bifidobacterium longum BL999 and prebiotics. Nutrition 2007;23:1-8.
12. Weizman Z, Alsheikh A. Safety and tolerance of a probiotic formula in early infancy comparing two probiotic agents: a pilot study. J Am Coll Nutr 2006;25:415-9.
13. Kitajima H, Sumida Y, Tanaka R, et al. Early administration of Bifidobacterium breve to preterm infants: randomised controlled trial. Arch Dis Child Fetal Neonatal Ed 1997;76:F101-7.
14. Costalos C, Skouteri V, Gounaris A, et al. Enteral feeding of premature infants with Saccharomyces boulardii. Early Hum Dev 2003;74:89-96.
15. Tako E, Glahn RP, Welch RM, et al. Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors, and storage protein and alters the microbiota in the pig intestine. Br J Nutr 2008;99:472-80.
16. Hoentjen F, Welling GW, Harmsen HJ, et al. Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with micro-flora changes and immunomodulation. Inflamm Bowel Dis 2005; 11:977-85.
17. Boehm G, Lidestri M, Casetta P, et al. Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants. Arch Dis Child Fetal Neonatal Ed 2002;86:F178-81.
18. Lidestri M, Agosti M, Marini A, et al. Oligosaccharides might stimulate calcium absorption in formula-fed preterm infants. Acta Paediatr Suppl 2003;91:91-2.
19. Fanaro S, Boehm G, Garssen J, et al. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr Suppl 2005;94:22-6.
20. Marini A, Negretti F, Boehm G, et al. Pro- and pre-biotics administration in preterm infants: colonization and influence on faecal flora. Acta Paediatr Suppl 2003;91:80-1.
21. Fanaro S, Jelinek J, Stahl B, et al. Acidic oligosaccharides from pectin hydrolysate as new component for infant formulae: effect on intestinal flora, stool characteristics, and pH. J Pediatr Gastroen-terol Nutr 2005;41:186-90.
22. Schmelzle H, Wirth S, Skopnik H, et al. Randomized double-blind study of the nutritional efficacy and bifidogenicity of a new infant formula containing partially hydrolyzed protein, a high β-palmitic acid level, and nondigestible oligosaccharides. J Pediatr Gastroenterol Nutr 2003;36:343-51.
23. Ziegler E, Vanderhoof JA, Petschow B, et al. Term infants fed formula supplemented with selected blends of prebiotics grow normally and have soft stools similar to those reported for breast-fed infants. J Pediatr Gastroenterol Nutr 2007;44:359-64.
24. Arslanoglu S, Moro GE, Boehm G. Early supplementation of prebiotic oligosaccharides protects formula-fed infants against infections during the first 6 months of life. J Nutr 2007; 137:2420-4.
25. Marcobal A, Underwood MA, Mills DA. Rapid determination of the bacterial composition of commercial probiotic products by terminal restriction fragment length polymorphism analysis. J Pediatr Gastroenterol Nutr 2008;46:608-11.
26. Sakamoto M, Hayashi H, Benno Y. Terminal restriction fragment length polymorphism analysis for human fecal microbiota and its application for analysis of complex bifidobacterial communities. Microbiol Immunol 2003;47:133-42.
27. Marsh TL, Saxman P, Cole J, et al. Terminal restriction fragment length polymorphism analysis program, a web-based research tool for microbial community analysis. Appl Environ Microbiol 2000;66:3616-20.
28. Liu WT, Marsh TL, Cheng H, et al. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 1997;63:4516-22.
29. Laroia S, Martin J. Methods for enumerating and propagating bifidobacteria. Cultured Dairy Products J 1991;26:32-3.
30. Chen HM, Lifschitz CH. Preparation of fecal samples for assay of volatile fatty acids by gas-liquid chromatography and high-performance liquid chromatography. Clin Chem 1989;35:74-6.
31. Miwa H, Yamamoto M. High-performance liquid chromatographic analysis of serum short-chain fatty acids by direct derivatization. J Chromatogr 1987;421:33-41.
32. Cole TJ. The LMS method for constructing normalized growth standards. Eur J Clin Nutr 1990;44:45-60.
33. Fenton TR. A new growth chart for preterm babies: Babson and Benda's chart updated with recent data and a new format. BMC Pediatr 2003;3:13.
34. Fenton TR, Sauve RS. Using the LMS method to calculate z-scores for the Fenton preterm infant growth chart. Eur J Clin Nutr 2007;61:1380-5.
35. Canganella F, Paganini S, Ovidi M, et al. A microbiology investigation on probiotic pharmaceutical products used for human health. Microbiol Res 1997;152:171-9.
36. Fasoli S, Marzotto M, Rizzotti L, et al. Bacterial composition of commercial probiotic products as evaluated by PCR-DGGE analysis. Int J Food Microbiol 2003;82:59-70.
37. Szajewska H, Fordymacka A, Bardowski J, et al. Microbiological and genetic analysis of probiotic products licensed for medicinal purposes. Med Sci Monit 2004;10:BR346-50.
38. Masco L, Huys G, De Brandt E, et al. Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 2005; 102:221-30.
39. Walsh MC, Kliegman RM. Necrotizing enterocolitis: treatment based on staging criteria. Pediatr Clin North Am 1986;33:179-201.
40. Deshpande G, Rao S, Patole S. Probiotics for prevention of necrotising enterocolitis in preterm neonates with very low birth-weight: a systematic review of randomised controlled trials. Lancet 2007;369:1614-20.
41. Hoyos AB. Reduced incidence of necrotizing enterocolitis associated with enteral administration of Lactobacillus acidophilus and Bifidobacterium infantis to neonates in an intensive care unit. Int J Infect Dis 1999;3:197-202.
42. Dani C, Biadaioli R, Bertini G, et al. Probiotics feeding in prevention of urinary tract infection, bacterial sepsis, and necrotizing enterocolitis in preterm infants. A prospective double-blind study. Biol Neonate 2002;82:103-8.
43. Lin HC, Su BH, Chen AC, et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2005;115:1-4.
44. Bin-Nun A, Bromiker R, Wilschanski M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr 2005;147:192-6.
45. Manzoni P, Mostert M, Leonessa ML, et al. Oral supplementation with Lactobacillus casei subspecies rhamnosus prevents enteric colonization by Candida species in preterm neonates: a randomized study. Clin Infect Dis 2006;42:1735-42.
46. Ward RE, Ninonuevo M, Mills DA, et al. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl Environ Microbiol 2006;72:4497-9.
47. Riedel CU, Foata F, Philippe D, et al. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-κB activation. World J Gastroenterol 2006;12:3729-35.
48. He F, Morita H, Ouwehand AC, et al. Stimulation of the secretion of pro-inflammatory cytokines by Bifidobacterium strains. Microbiol Immunol 2002;46:781-5.
49. Ott SJ, Musfeldt M, Timmis KN, et al. In vitro alterations of intestinal bacterial microbiota in fecal samples during storage. Diagn Microbiol Infect Dis 2004;50:237-45.
50. Rochet V, Rigottier-Gois L, Rabot S, et al. Validation of fluorescent in situ hybridization combined with flow cytometry for assessing interindividual variation in the composition of human fecal micro-flora during long-term storage of samples. J Microbiol Methods 2004;59:263-70.
51. Cooke RJ, Ainsworth SB, Fenton AC. Postnatal growth retardation: a universal problem in preterm infants. Arch Dis Child Fetal Neonatal Ed 2004;89:F428-30.
52. Backhed F, Ding H, Wang T, et al. The Gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004;101:15718-23.
53. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated Gut microbiome with increased capacity for energy harvest. Nature 2006;444:1027-31.
54. Brookes ST, Whitley E, Peters TJ, et al. Subgroup analyses in randomised controlled trials: quantifying the risks of false-positives and false-negatives. Health Technol Assess 2001;5:1-56.
55. Wong JM, de Souza R, Kendall CW, et al. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 2006; 40:235-43.
56. Cook SI, Sellin JH. Review article: short chain fatty acids in health and disease. Aliment Pharmacol Ther 1998;12:499-507.
57. Boehm G, Jelinek J, Stahl B, et al. Prebiotics in infant formulas. J Clin Gastroenterol 2004;38:S76-9.
58. Wang C, Shoji H, Sato H, et al. Effects of oral administration of Bifidobacterium breve on fecal lactic acid and short-chain fatty acids in low birth weight infants. J Pediatr Gastroenterol Nutr 2007;44:252-7.
59. Waligora-Dupriet AJ, Dugay A, Auzeil N, et al. Evidence for clostridial implication in necrotizing enterocolitis through bacterial fermentation in a gnotobiotic quail model. Pediatr Res 2005; 58:629-35.
60. Pender SL, Quinn JJ, Sanderson IR, et al. Butyrate upregulates stromelysin-1 production by intestinal mesenchymal cells. Am J Physiol Gastrointest Liver Physiol 2000;279:G918-24.
61. Cummings JH. Short chain fatty acids in the human colon. Gut 1981;22:763-79.
62. Kliegman RM, Willoughby RE. Prevention of necrotizing enter-ocolitis with probiotics. Pediatrics 2005;115:171-2.
63. Bell EF. Preventing necrotizing enterocolitis: what works and how safe? Pediatrics 2005;115:173-4.