Modulation of the gut microbiota with antibiotic treatment suppresses whole body urea production in neonatal pigs

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 3, 2013, Pages

  Puiman, Patrycja ^a,b   Stoll, Barbara ^b   Mølbak, Lars ^c   de Bruijn, Adrianus ^a   Schierbeek, Henk ^a   Boye, Mette ^c   Boehm, Günther ^a,d   Renes, Ingrid ^a   van Goudoever, Johannes ^a,e,f   Burrin, Douglas ^b  

^a SOPHIA CHILDREN S HOSPITAL   (Netherlands)

^b CHILDREN S NUTRITION RESEARCH CENTER   (United States)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d Centre for Specialized Nutrition   (Germany)

^e EMMA CHILDREN S HOSPITAL   (Netherlands)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Amino acids; Bifidobacteria; Intestine; Metabolism; Threonine

Indexed keywords

AMINO ACID; AMPICILLIN; ANTIBIOTIC AGENT; BUTORPHANOL TARTRATE; GENTAMICIN; ISOTOPE; METRONIDAZOLE; NITROGEN; PROBIOTIC AGENT; THREONINE; UREA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; COLON; CONTROLLED STUDY; HYPOTHESIS; INTESTINE FLORA; MODULATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SMALL INTESTINE; SWINE; UREA CYCLE; WESTERN BLOTTING;

AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; ANTI-BACTERIAL AGENTS; BIFIDOBACTERIUM; BLOTTING, WESTERN; BODY WEIGHT; GASTROINTESTINAL TRACT; IMMUNOHISTOCHEMISTRY; KINETICS; METAGENOME; MUCIN-2; MUCINS; NITROGEN; ORGAN SIZE; OXIDATION-REDUCTION; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PROBIOTICS; PROTEIN BIOSYNTHESIS; SWINE; THREONINE; UREA;

EID: 84873395667     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00229.2011     Document Type: Article

References (56)

1. Alfaleh K, Anabrees J, Bassler D. Probiotics reduce the risk of necro-tizing enterocolitis in preterm infants: a meta-analysis. Neonatology 97: 93-99, 2010.
2. Alfaleh K, Bassler D. Probiotics for prevention of necrotizing enteroco-litis in preterm infants. Cochrane Database Syst Rev CD005496, 2008.
3. Allen A, Hutton DA, Pearson JP. The MUC2 gene product: a human intestinal mucin. Int J Biochem Cell Biol 30: 797-801, 1998.
4. Anand RJ, Leaphart CL, Mollen KP, Hackam DJ. The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock 27: 124-133, 2007.
5. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 307: 1915-1920, 2005.
6. Brunton L, Chabner B, Knollman B. Goodman and Gilman's The Pharmacological Basis of Therapeutics. New York, NY: McGraw-Hill, 2011.
7. Burrin DG, Stoll B, Jiang R, Petersen Y, Elnif J, Buddington RK, Schmidt M, Holst JJ, Hartmann B, Sangild PT. GLP-2 stimulates intestinal growth in premature TPN-fed pigs by suppressing proteolysis and apoptosis. Am J Physiol Gastrointest Liver Physiol 279: G1249- G1256, 2000.
8. Chen LX, Yin YL, Jobgen WS, Jobgen SC, Knabe DA, Hu WXGW. In vitro oxidation of essential amino acids by jejunal mucosal cells of growing pigs. Livestock Science 19-23, 2007.
9. Collado MC, Meriluoto J, Salminen S. Development of new probiotics by strain combinations: is it possible to improve the adhesion to intestinal mucus? J Dairy Sci 90: 2710-2716, 2007.
10. Cooney RN, Kimball SR, Vary TC. Regulation of skeletal muscle protein turnover during sepsis: mechanisms and mediators. Shock 7: 1-16, 1997.
11. Dai ZL, Wu G, Zhu WY. Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Frontiers Biosci 16: 1768- 1786, 2011.
12. Deshpande G, Rao S, Patole S. Probiotics for prevention of necrotising enterocolitis in preterm neonates with very low birthweight: a systematic review of randomised controlled trials. Lancet 369: 1614-1620, 2007.
13. Fujii T, Ohtsuka Y, Lee T, Kudo T, Shoji H, Sato H, Nagata S, Shimizu T, Yamashiro Y. Bifidobacterium breve enhances transforming growth factor beta1 signaling by regulating Smad7 expression in preterm infants. J Pediatr Gastroenterol Nutr 43: 83-88, 2006.
14. Fuller MF, Reeds PJ. Nitrogen cycling in the gut. Annu Rev Nutr 18: 385-411, 1998.
15. Gum JR Jr, Hicks JW, Toribara NW, Rothe EM, Lagace RE, Kim YS. The human MUC2 intestinal mucin has cysteine-rich subdomains located both upstream and downstream of its central repetitive region. J Biol Chem 267: 21375-21383, 1992.
16. Hay WW Jr. Nutrient supplies for optimal health in preterm infants. J Pediatr Gastroenterol Nutr 45, Suppl 3: S163-S169, 2007.
17. Hulst JM, van Goudoever JB, Zimmermann LJ, Hop WC, Albers MJ, Tibboel D, Joosten KF. The effect of cumulative energy and protein deficiency on anthropometric parameters in a pediatric ICU population. Clin Nutr 23: 1381-1389, 2004.
18. Jackson AA, Gibson NR, Bundy R, Hounslow A, Millward DJ, Wootton SA. Transfer of (15)N from oral lactose-ureide to lysine in normal adults. Int J Food Sci Nutr 55: 455-462, 2004.
19. Juntunen M, Kirjavainen PV, Ouwehand AC, Salminen SJ, Isolauri E. Adherence of probiotic bacteria to human intestinal mucus in healthy infants and during rotavirus infection. Clin Diagnostic Lab Immunol 8: 293-296, 2001.
20. Kuehl CJ, Wood HD, Marsh TL, Schmidt TM, Young VB. Colonization of the cecal mucosa by Helicobacter hepaticus impacts the diversity of the indigenous microbiota. Infect Immun 73: 6952-6961, 2005.
21. Lang CH, Frost RA, Vary TC. Regulation of muscle protein synthesis during sepsis and inflammation. Am J Physiol Endocrinol Metab 293: E453-E459, 2007.
22. Larroque B, Ancel PY, Marret S, Marchand L, Andre M, Arnaud C, Pierrat V, Roze JC, Messer J, Thiriez G, Burguet A, Picaud JC, Breart G, Kaminski M. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet 371: 813-820, 2008.
23. Law GK, Bertolo RF, Adjiri-Awere A, Pencharz PB, Ball RO. Adequate oral threonine is critical for mucin production and gut function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 292: G1293-G1301, 2007.
24. Le Floc'h N, Obled C, Seve B. In vivo threonine oxidation rate is dependent on threonine dietary supply in growing pigs fed low to adequate levels. J Nutr 125: 2550-2562, 1995.
25. Leser TD, Lindecrona RH, Jensen TK, Jensen BB, Moller K. Changes in bacterial community structure in the colon of pigs fed different experimental diets and after infection with Brachyspira hyodysenteriae. Appl Environ Microbiol 66: 3290-3296, 2000.
26. Lien KA, Sauer WC, Fenton M. Mucin output in ileal digesta of pigs fed a protein-free diet. Z Ernahrungswiss 36: 182-190, 1997.
27. Madsen K. Probiotics and the immune response. J Clin Gastroenterol 40: 232-234, 2006.
28. Mantle M, Allen A. Isolation and characterization of the native glyco-protein from pig small-intestinal mucus. Biochem J 195: 267-275, 1981.
29. Metges CC. Contribution of microbial amino acids to amino acid homeo-stasis of the host. J Nutr 130: 1857S-1864S, 2000.
30. Metges CC, Eberhard M, Petzke KJ. Synthesis and absorption of intestinal microbial lysine in humans and non-ruminant animals and impact on human estimated average requirement of dietary lysine. Curr Opin Clin Nutr Metab Care 9: 37-41, 2006.
31. Metges CC, El-Khoury AE, Henneman L, Petzke KJ, Grant I, Bedri S, Pereira PP, Ajami AM, Fuller MF, Young VR. Availability of intestinal microbial lysine for whole body lysine homeostasis in human subjects. Am J Physiol Endocrinol Metab 277: E597-E607, 1999.
32. Metges CC, Petzke KJ, El-Khoury AE, Henneman L, Grant I, Bedri S, Regan MM, Fuller MF, Young VR. Incorporation of urea and ammonia nitrogen into ileal and fecal microbial proteins and plasma free amino acids in normal men and ileostomates. Am J Clin Nutr 70: 1046-1058, 1999.
33. Metges CC, Petzke KJ, Hennig U. Gas chromatography/combustion/ isotope ratio mass spectrometric comparison of N-acetyl- and N-pivaloyl amino acid esters to measure 15N isotopic abundances in physiological samples: a pilot study on amino acid synthesis in the upper gastro-intestinal tract of minipigs. J Mass Spectrom 31: 367-376, 1996.
34. Mohan R, Koebnick C, Schildt J, Schmidt S, Mueller M, Possner M, Radke M, Blaut M. Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: a double-blind, placebo-controlled, randomized study. J Clin Microbiol 44: 4025-4031, 2006.
35. Molbak L, Thomsen LE, Jensen TK, Bach Knudsen KE, Boye M. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. J Appl Microbiol 103: 1853-1867, 2007.
36. Nichols NL, Bertolo RF. Luminal threonine concentration acutely affects intestinal mucosal protein and mucin synthesis in piglets. J Nutr 138: 1298-1303, 2008.
37. Niinikoski H, Stoll B, Guan X, Kansagra K, Lambert BD, Stephens J, Hartmann B, Holst JJ, Burrin DG. Onset of small intestinal atrophy is associated with reduced intestinal blood flow in TPN-fed neonatal piglets. J Nutr 134: 1467-1474, 2004.
38. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol 5: e177, 2007.
39. Schaart MW, de Bruijn AC, Schierbeek H, Tibboel D, Renes IB, van Goudoever JB. Small intestinal MUC2 synthesis in human preterm infants. Am J Physiol Gastrointest Liver Physiol 296: G1085-G1090, 2009.
40. Schaart MW, Schierbeek H, de Bruijn AC, Tibboel D, van Goudoever JB, Renes IB. A novel method to determine small intestinal barrier function in human neonates in vivo. Gut 55: 1366-1367, 2006.
41. Schaart MW, Schierbeek H, van der Schoor SR, Stoll B, Burrin DG, Reeds PJ, van Goudoever JB. Threonine utilization is high in the intestine of piglets. J Nutr 135: 765-770, 2005.
42. 13C]bicarbonate infusion for measurement of CO2 production. Am J Physiol Endocrinol Metab 268: E1123-E1127, 1995.
43. Stoll B, Burrin DG. Measuring splanchnic amino acid metabolism in vivo using stable isotopic tracers. J Anim Sci Suppl 84: E60-E72, 2006.
44. Stoll B, Chang X, Fan MZ, Reeds PJ, Burrin DG. Enteral nutrient intake level determines intestinal protein synthesis and accretion rates in neonatal pigs. Am J Physiol Gastrointest Liver Physiol 279: G288-G294, 2000.
45. Stoll B, Price PT, Reeds PJ, Chang X, Henry JF, van Goudoever JB, Holst JJ, Burrin DG. Feeding an elemental diet vs a milk-based formula does not decrease intestinal mucosal growth in infant pigs. J Parenter Enteral Nutr 30: 32-39, 2006.
46. Toribara NW, Gum JR Jr, Culhane PJ, Lagace RE, Hicks JW, Petersen GM, Kim YS. MUC-2 human small intestinal mucin gene structure Repeated arrays and polymorphism. J Clin Invest 88: 1005-1013, 1991.
47. Torrallardona D, Harris CI, Fuller MF. Lysine synthesized by the gastrointestinal microflora of pigs is absorbed, mostly in the small intestine. Am J Physiol Endocrinol Metab 284: E1177-E1180, 2003.
48. Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol 587: 4153-4158, 2009.
49. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031, 2006.
50. Tytgat KM, Buller HA, Opdam FJ, Kim YS, Einerhand AW, Dekker J. Biosynthesis of human colonic mucin: Muc2 is the prominent secretory mucin. Gastroenterology 107: 1352-1363, 1994.
51. van der Schoor SR, Wattimena DL, Huijmans J, Vermes A, van Goudoever JB. The gut takes nearly all: threonine kinetics in infants. Am J Clin Nutr 86: 1132-1138, 2007.
52. van Goudoever JB, Stoll B, Henry JF, Burrin DG, Reeds PJ. Adaptive regulation of intestinal lysine metabolism. Proc Natl Acad Sci USA 97: 11620-11625, 2000.
53. Vann RC, Nguyen HV, Reeds PJ, Burrin DG, Fiorotto ML, Steele NC, Deaver DR, Davis TA. Somatotropin increases protein balance by lowering body protein degradation in fed, growing pigs. Am J Physiol Endocrinol Metab 278: E477-E483, 2000.
54. Vary TC, Kimball SR. Regulation of hepatic protein synthesis in chronic inflammation and sepsis. Am J Physiol Cell Physiol 262: C445-C452, 1992.
55. Wang C, Shoji H, Sato H, Nagata S, Ohtsuka Y, Shimizu T, Ya-mashiro Y. 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 44: 252-257, 2007.
56. Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM. The intestinal bacterial colonisation in preterm infants: a review of the literature. Clin Nutr 25: 361-368, 2006.