Infant formula supplemented with polyamines alters the intestinal microbiota in neonatal BALB/cOlaHsd mice

Journal of Nutritional Biochemistry

Volumn 23, Issue 11, 2012, Pages 1508-1513

  Gómez Gallego, Carlos ^a   Collado, María C ^b   Ilo, Toni ^c   Jaakkola, Ulla Marjut ^c   Bernal, María J ^d   Periago, María J ^a   Salminen, Seppo ^e   Ros, Gaspar ^a   Frias, Rafael ^c  

^a UNIVERSITY OF MURCIA   (Spain)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^c UNIVERSITY OF TURKU   (Finland)

^d Institute of Infant Nutrition Hero Spain   (Spain)

^e UNIVERSITY OF TURKU   (Finland)

Author keywords

BALB c; Breastfeeding; Infant formula; Microbiota; Polyamines; Putrescine; Spermidine; Spermine

Indexed keywords

PUTRESCINE; SPERMIDINE; SPERMINE;

AKKERMANSIA; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL MILK; BACTERIUM; BIFIDOBACTERIUM; ENTEROCOCCUS; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; INTESTINE FLORA; LACTOBACILLUS; MOUSE; NEWBORN; NONHUMAN;

ANIMALS; ANIMALS, NEWBORN; BIFIDOBACTERIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTEROCOCCUS; FEMALE; INFANT FORMULA; INTESTINES; LACTOBACILLUS; MALE; METAGENOME; MICE; MICE, INBRED BALB C; POLYAMINES; PUTRESCINE; SPERMIDINE; SPERMINE; WEANING;

AKKERMANSIA; BIFIDOBACTERIUM; ENTEROCOCCUS; LACTOBACILLUS; MUS;

EID: 84867705864     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2011.10.003     Document Type: Article

References (47)

1. Baró L., Jiménez J., Martínez-Férez A., Boza J.J. Bioactive compounds derived from human milk. Ars Pharmaceutica 2001, 42(1):21-38.
2. Goldman A.S. Modulation of the gastrointestinal tract of infants by human milk interfaces and interactions. An evolutionary perspective. J Nutr 2000, 130:426-431.
3. Gueimonde M., Laitinen K., Salminen S., Isolauri E. Breast milk: a source of bifidobacteria for infant gut development and maturation?. Neonatology 2007, 92(1):64-66.
4. Newburg D.S., Walker W.A. Protection of the neonate by the innate immune system of developing gut and of human milk. Ped Res 2007, 61:2-8.
5. Löser C. Polyamines in human and animal milk. Br J Nutr 2000, 84(1):55-58.
6. Jolois O., Peulen O., Collin S., Simons M., Dandrifosse G., Heinen E. Spermine induces precocious development of the spleen in mice. Exp Physiol 2002, 87(1):69-75.
7. Steege J.C.A., Buurman W.A., Forget P.P. Spermine induces maturation of the immature intestinal immune system in neonatal mice. J Ped Gastroenterol Nutr 1997, 25(3):332-340.
8. Larqué E., Sabater-Molina M., Zamora S. Biological significance of dietary polyamines. Nutrition 2007, 23:87-95.
9. Seiler N., Raul F. Polyamines and the intestinal tract. Crit Rev Clin Lab Sci 2007, 44:365-411.
10. Ferioli M.E., Pirona L., Pinotti O. Prolactin and polyamine catabolism: specific effect on polyamine oxidase activity in rat thymus. Mol Cell Endo 2000, 165(1-2):51-56.
11. Löser C., Eisel A., Harms D., Fölsch U.R. Dietary polyamines are essential luminal growth factors for small intestinal and colonic mucosal growth and development. Gut 1999, 44(1):12-16.
12. Guo X., Rao J.N., Liu L., Zou T.T., Turner D.J., Bass B.L., et al. Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol 2003, 285:1174-1187.
13. Wang J.Y. Polyamines regulate expression of E-cadherin and play an important role in control of intestinal epithelial barrier function. Inflammopharmacol 2005, 13:91-101.
14. Dandrifosse G., Peulen O., El Khefif N., Deloyer P., Dandrifosse A.C., Grandfils C. Are milk polyamines preventive agents against food allergy?. Proc Nutr Soc 2000, 59:81-86.
15. Le Huërou-Luron I., Blat S., Boudry G. Breast- v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev 2010, 23(1):23-36.
16. Peulen O., Dewé W., Dandrifosse G., Henrotay I., Romain N. The relationship between spermine content of human milk during the first postnatal month and allergy in children. Pub Health Nutr 1998, 1(3):181-184.
17. WHO and UNICEF, 2003. Global strategy for infant and young child feeding, ISBN: 92 4 156221 8. http://www.who.int/nutrition/publications/infantfeeding/9241562218/en/index.html.
18. Buts J.P., De Keyser N., De Raedemaeker L., Collette E., Sokal E.M. Polyamine profiles in human milk, infant artificial formulas, and semi-elemental diets. J Ped Gastro Nut 1995, 21(1):44-49.
19. Pollack P.F., Koldousky O., Nishioka F. Polyamines in human and rat milk and in infant formulas. Am J Clin Nutr 1992, 56:371-375.
20. Romain N., Dandrifosse G., Jeusette F., Forget P. Polyamine concentration in rat milk and food, human-milk, and infant formulas. Ped Res 1992, 32(1):58-63.
21. Nicklas W., Baneux P., Boot R., Decelle T., Deeny A.A., Fumanelli M., et al. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002, 36(1):20-42.
22. Collado M.C., Derrien M., Isolauri E., de Vos W.M., Salminen S. Intestinal integrity and Akkermansia muciniphila: a mucin-degrading member of the intestinal microbiota present in infants, adults and the elderly. Appl Environ Microbiol 2007, 73(23):7767-7770.
23. Commission directive 2006/141/EC of 22 December 2006 on infant formulae and follow-on formulae and amending directive 1999/21/EC.
24. Koletzko B., Baker S., Cleghorn G., Fagundes Neto U., Gopalan S., Hernell O., et al. Global standard for the composition of infant formula: recommendations of an ESPGHAN Coordinate International Expert Group. J Ped Gastr Nutr 2005, 41:584-599.
25. Til H.P., Falke H.E., Prinsent M.K., Willems M.I. Acute and subacute toxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats. Food Chem Toxicol 1997, 35:337-348.
26. Kalliomäki M., Collado M.C., Salminen S., Isolauri E. Early differences in faecal microbiota composition in children may predict later weight-gain?. Am J Clin Nutr 2008, 87:534-538.
27. Rigottier-Gois L., Le Bourhis A.G., Gramet G., Rochet V., Doré J. Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human faeces using 16S rRNA probes. FEMS Microb Ecol 2003, 43:237-245.
28. Amann R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R., Stahl D.A., Olson R.J. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 1990, 56:1919-1925.
29. Langendijk P.S., Schut F., Jansen G.J., Raangs G.C., Kamphuis G.R., Wilkinson M.H.F., Welling G.W. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 1995, 61:3069-3075.
30. Manz W., Amann R., Ludwig W., Vancanneyt M., Schleifer K.H. Application of a suite of 16S rRNA-specific oligonucleotides probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 1996, 142:1097-1106.
31. Franks A.H., Harmsen H.J.M., Raangs G.C., Jansen G.J., Schut F., Welling G.W. Variations of bacterial populations in human feces quantified by fluorescence in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 1998, 64:3336-3345.
32. Harmsen H.J.M., Elfferich P., Schut F., Welling G.W. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb Ecol Health Dis 1999, 11:3-12.
33. Bezirtzoglou E., Tsiotsias A., Welling G.W. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 2011, 10.1016/j.anaerobe.2011.03.009.
34. Echarri P.P., Graciá C.M., Berruezo G.R., Vives I., Ballesta M., Solís G., Morillas I.V., Reyes-Gavilán C.G., Margolles A., Gueimonde M. Assessment of intestinal microbiota of full-term breast-fed infants from two different geographical locations. Early Hum Dev 2011, 87(7):511-513.
35. Collado M.C., Sanz Y. Quantification of mucosa-adhered microbiota of lambs and calves by the use of culture methods and fluorescent in situ hybridization coupled with flow cytometry techniques. Vet Microbiol 2007, 121:229-306.
36. LeBouder E., Rey-Nores J.E., Raby A.C., Affolter M., Vidal K., Thornton C.A., Labéta M.O. Modulation of neonatal microbial recognition: TLR-mediated innate immune responses are specifically and differentially modulated by human milk. J Inmunol 2006, 176(6):3742-3752.
37. Cani P.D., Neyrinck A.M., Fava F., Knauf C., Burcelin R.G., Tuohy K.M., Gibson G.R., Delzenne N.M. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007, 50:2374-2383.
38. Bardocz S. Polyamines in food and their consequences for food quality and human health. Trends in Food Sci & Technol 1995, 61:341-346.
39. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444(7121):860-867.
40. Kalliomäki M., Kirjavainen P., Eerola E., Kero P., Salminen S., Isolauri E. Distinct patterns of neonatal gut microflora in infants developing or not developing atopy. J Allergy Clin Immunol 2001, 107:129-134.
41. Harmsen H.J., Wildeboer-Veloo A.C., Raangs G.C., Wagendorp A.A., Klijn N., Bindels J.G., Wagendorp A.A., Klijn N., Welling G.W. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Ped Gastro and Nut 2000, 30(1):61-67.
42. Derrien M., van Passel M.W., van de Bovenkamp J.H., Schipper R.G., de Vos W.M., Dekker J. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes 2010, 1(4):254-268.
43. Swidsinski A., Dörffel Y., Loening-Baucke V., Theissig F., Rückert J.C., Ismail M., Rau W.A., Gaschler D., Weizenegger M., Kühn S., Schilling J., Dörffel W.V. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 2011, 60(1):34-40.
44. Campieri M., Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut 2001, 48(1):132-135.
45. Shih D.Q., Targan S.R. Immunopathogenesis of inflammatory bowel disease. W J Gastro 2008, 14(3):390-400.
46. Sonoyama K., Fujiwara R., Takemura N., Watanabe J., Ito H., Morita T. Response of gut microbiota to fasting and hibernation in Syrian hamsters. App Env Microbiol 2009, 75(20):6451-6456.
47. Sonoyama K., Ogasawara T., Goto H., Yoshida T., Takemura N., Fujiwara R., Watanabe J., Ito H., Morita T., Tokunaga Y., Yanagihara T. Comparison of gut microbiota and allergic reactions in BALB/c mice fed different cultivars of rice. Brit J Nutr 2010, 103(2):218-226.