Branched chain fatty acids reduce the incidence of necrotizing enterocolitis and alter gastrointestinal microbial ecology in a neonatal rat model

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Ran Ressler, Rinat R ^a   Khailova, Ludmila ^b   Arganbright, Kelly M ^b   Adkins Rieck, Camille K ^b   Jouni, Zeina E ^c   Koren, Omry ^a   Ley, Ruth E ^a   Brenna, J Thomas ^a   Dvorak, Bohuslav ^b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c Mead Johnson Nutritionals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN FATTY ACID; FATTY ACID; RNA 16S; UNCLASSIFIED DRUG; INTERLEUKIN 10; MESSENGER RNA; MUCIN; NEUROPEPTIDE; PEPTIDE; PHOSPHOLIPID; TFF3 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACILLUS SUBTILIS; BLOOD ANALYSIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; FAT INTAKE; GENE; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC MARKER; IMMUNOHISTOCHEMISTRY; INFECTION RISK; INTERLEUKIN 10 GENE; INTESTINE FLORA; MUCIN GENE; NECROTIZING ENTEROCOLITIS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOMONAS AERUGINOSA; PUP (RODENT); PYROSEQUENCING; RAT; RNA GENE; THERAPY EFFECT; ANIMAL; BACTERIUM; BLOOD; CHEMISTRY; DIET; DISEASE MODEL; DRUG EFFECT; GAS CHROMATOGRAPHY; GASTROINTESTINAL TRACT; GENETIC VARIABILITY; GENETICS; HEALTH; ILEUM; INCIDENCE; LIVER; METABOLISM; MICROBIOLOGY; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; BACTERIA; CHROMATOGRAPHY, GAS; DIET; DISEASE MODELS, ANIMAL; ENTEROCOLITIS, NECROTIZING; FATTY ACIDS; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETIC VARIATION; HEALTH; ILEUM; IMMUNOHISTOCHEMISTRY; INCIDENCE; INTERLEUKIN-10; LIVER; MUCINS; NEUROPEPTIDES; PEPTIDES; PHOSPHOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 83355176327     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029032     Document Type: Article

References (72)

1. Egge H, Murawski U, Ryhage R, Gyorgy P, Chatranon W, et al. (1972) Minor constituents of human milk. IV. Analysis of the branched chain fatty acids. Chem Phys Lipids 8: 42-55.
2. Gibson RA, Kneebone GM, (1981) Fatty acid composition of human colostrum and mature breast milk. Am J Clin Nutr 34: 252-257.
3. Ran-Ressler RR, Sim D, O'Donnell-Megaro AM, Bauman DE, Barbano DM, et al. (2011) Branched chain fatty acid content of united states retail cow's milk and implications for dietary intake. Lipids 46: 569-576.
4. Kaneda T, (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55: 288-302.
5. Veerkamp JH, (1971) Fatty acid composition of Bifidobacterium and Lactobacillus strains. J Bacteriol 108: 861-867.
6. Bezirtzoglou E, Maipa V, Chotoura N, Apazidou E, Tsiotsias A, et al. (2006) Occurrence of Bifidobacterium in the intestine of newborns by fluorescence in situ hybridization. Comp Immunol Microbiol Infect Dis 29: 345-352.
7. Hall MA, Cole CB, Smith SL, Fuller R, Rolles CJ, (1990) Factors influencing the presence of faecal lactobacilli in early infancy. Arch Dis Child 65: 185-188.
8. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, et al. (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108 (Suppl 1): 4578-4585.
9. Nicolaides N, Ray T, (1965) Skin Lipids. 3. Fatty Chains in Skin Lipids. The Use of Vernix Caseosa to Differentiate between Endogenous and Exogenous Components in Human Skin Surface Lipid. J Am Oil Chem Soc 42: 702-707.
10. Pickens WL, Warner RR, Boissy YL, Boissy RE, Hoath SB, (2000) Characterization of vernix caseosa: water content, morphology, and elemental analysis. J Invest Dermatol 115: 875-881.
11. Rissmann R, Groenink HW, Weerheim AM, Hoath SB, Ponec M, et al. (2006) New insights into ultrastructure, lipid composition and organization of vernix caseosa. J Invest Dermatol 126: 1823-1833.
12. Narendran V, Wickett RR, Pickens WL, Hoath SB, (2000) Interaction between pulmonary surfactant and vernix: a potential mechanism for induction of amniotic fluid turbidity. Pediatr Res 48: 120-124.
13. Miettinen TA, Luukkainen T, (1968) Gas-liquid chromatographic and mass spectrometric studies on sterols in vernix caseosa, amniotic fluid and meconium. Acta Chem Scand 22: 2603-2612.
14. Biezenski JJ, Pomerance W, Goodman J, (1968) Studies on the origin of amniotic fluid lipids. I. Normal composition. Am J Obstet Gynecol 102: 853-861.
15. Ran-Ressler RR, Devapatla S, Lawrence P, Brenna JT, (2008) Branched chain fatty acids are constituents of the normal healthy newborn gastrointestinal tract. Pediatr Res 64: 605-609.
16. Pritchard JA, (1966) Fetal swallowing and amniotic fluid volume. Obstet Gynecol 28: 606-610.
17. Neu J, Walker WA, (2011) Necrotizing enterocolitis. N Engl J Med 364: 255-264.
18. Lin PW, Stoll BJ, (2006) Necrotising enterocolitis. Lancet 368: 1271-1283.
19. Grave GD, Nelson SA, Walker WA, Moss RL, Dvorak B, et al. (2007) New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr Res 62: 510-514.
20. Caplan MS, Jilling T, (2001) New concepts in necrotizing enterocolitis. Curr Opin Pediatr 13: 111-115.
21. Claud EC, Walker WA, (2001) Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 15: 1398-1403.
22. Young CM, Kingma SD, Neu J, (2011) Ischemia-reperfusion and neonatal intestinal injury. J Pediatr 158: e25-28.
23. Cilieborg MS, Boye M, Thymann T, Jensen BB, Sangild PT, (2011) Diet-dependent effects of minimal enteral nutrition on intestinal function and necrotizing enterocolitis in preterm pigs. JPEN J Parenter Enteral Nutr 35: 32-42.
24. Cilieborg MS, Thymann T, Siggers R, Boye M, Bering SB, et al. (2011) The incidence of necrotizing enterocolitis is increased following probiotic administration to preterm pigs. J Nutr 141: 223-230.
25. Frost BL, Caplan MS, (2011) Probiotics and prevention of neonatal necrotizing enterocolitis. Curr Opin Pediatr 23: 151-155.
26. McGuire W, Anthony MY, (2003) Donor human milk versus formula for preventing necrotising enterocolitis in preterm infants: systematic review. Arch Dis Child Fetal Neonatal Ed 88: F11-F14.
27. Lucas A, Cole TJ, (1990) Breast milk and neonatal necrotising enterocolitis. Lancet 336: 1519-1523.
28. Caplan MS, Russell T, Xiao Y, Amer M, Kaup S, et al. (2001) Effect of polyunsaturated fatty acid (PUFA) supplementation on intestinal inflammation and necrotizing enterocolitis (NEC) in a neonatal rat model. Pediatr Res 49: 647-652.
29. Carlson SE, Montalto MB, Ponder DL, Werkman SH, Korones SB, (1998) Lower incidence of necrotizing enterocolitis in infants fed a preterm formula with egg phospholipids. Pediatr Res 44: 491-498.
30. Beeby PJ, Jeffery H, (1992) Risk factors for necrotising enterocolitis: the influence of gestational age. Arch Dis Child 67: 432-435.
31. Magne F, Suau A, Pochart P, Desjeux JF, (2005) Fecal microbial community in preterm infants. J Pediatr Gastroenterol Nutr 41: 386-392.
32. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, et al. (2009) 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 3: 944-954.
33. Patterson JK, Yasuda K, Welch RM, Miller DD, Lei XG, (2010) Supplemental dietary inulin of variable chain lengths alters intestinal bacterial populations in young pigs. J Nutr 140: 2158-2161.
34. Bezirtzoglou E, Stavropoulou E, (2011) Immunology and probiotic impact of the newborn and young children intestinal microflora. Anaerobe Apr 16 epub.
35. Campeotto F, Suau A, Kapel N, Magne F, Viallon V, et al. (2011) A fermented formula in pre-term infants: clinical tolerance, gut microbiota, down-regulation of faecal calprotectin and up-regulation of faecal secretory IgA. Br J Nutr pp. 1-10.
36. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J, (2011) Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS One 5: e15046.
37. Zimmermann MB, Chassard C, Rohner F, N'Goran EK, Nindjin C, et al. (2011) The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Cote d'Ivoire. Am J Clin Nutr 92: 1406-1415.
38. Ravussin Y, Koren O, Spor A, Leduc C, Gutman R, et al. (2011) Responses of Gut Microbiota to Diet Composition and Weight Loss in Lean and Obese Mice. Obesity (Silver Spring) in press.
39. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI, (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213-223.
40. Dvorak B, McWilliam DL, Williams CS, Dominguez JA, Machen NW, et al. (2000) Artificial formula induces precocious maturation of the small intestine of artificially reared suckling rats. J Pediatr Gastroenterol Nutr 31: 162-169.
41. Baguma-Nibasheka M, Brenna JT, Nathanielsz PW, (1999) Delay of preterm delivery in sheep by omega-3 long-chain polyunsaturates. Biol Reprod 60: 698-701.
42. Khailova L, Dvorak K, Arganbright KM, Halpern MD, Kinouchi T, et al. (2009) Bifidobacterium Bifidum Improves Intestinal Integrity in a Rat Model of Necrotizing Enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G940-G949.
43. Clark JA, Doelle SM, Halpern MD, Saunders TA, Holubec H, et al. (2006) Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. Am J Physiol Gastrointest Liver Physiol 291: G938-G949.
44. Dvorak B, Halpern MD, Holubec H, Williams CS, McWilliam DL, et al. (2002) Epidermal growth factor reduces the development of necrotizing enterocolitis in a neonatal rat model. Am J Physiol Gastrointest Liver Physiol 282: G156-G164.
45. Koren O, Spor A, Felin J, Fak F, Stombaugh J, et al. (2011) Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A 108 (Suppl 1): 4592-4598.
46. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R, (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5: 235-237.
47. Reeder J, Knight R, (2011) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668-669.
48. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2011) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
49. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
50. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
51. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
52. Dvorak B, Halpern MD, Holubec H, Dvorakova K, Dominguez JA, et al. (2003) Maternal milk reduces severity of necrotizing enterocolitis and increases intestinal IL-10 in a neonatal rat model. Pediatr Res 53: 426-433.
53. Siggers RH, Siggers J, Boye M, Thymann T, Molbak L, et al. (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138: 1437-1444.
54. Lu J, Jilling T, Li D, Caplan MS, (2007) Polyunsaturated fatty acid supplementation alters proinflammatory gene expression and reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Pediatr Res 61: 427-432.
55. Caplan MS, Miller-Catchpole R, Kaup S, Russell T, Lickerman M, et al. (1999) Bifidobacterial supplementation reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Gastroenterology 117: 577-583.
56. Chao J, Wolfaardt GM, Arts MT, (2011) Characterization of Pseudomonas aeruginosa fatty acid profiles in biofilms and batch planktonic cultures. Can J Microbiol 56: 1028-1039.
57. Conrad RS, Gilleland HE Jr, (1981) Lipid alterations in cell envelopes of polymyxin-resistant Pseudomonas aeruginosa isolates. J Bacteriol 148: 487-497.
58. Huang JM, La Ragione RM, Nunez A, Cutting SM, (2008) Immunostimulatory activity of Bacillus spores. FEMS Immunol Med Microbiol 53: 195-203.
59. Selvam R, Maheswari P, Kavitha P, Ravichandran M, Sas B, et al. (2009) Effect of Bacillus subtilis PB6, a natural probiotic on colon mucosal inflammation and plasma cytokines levels in inflammatory bowel disease. Indian J Biochem Biophys 46: 79-85.
60. Sun P, Wang JQ, Zhang HT, (2011) Effects of Bacillus subtilis natto on performance and immune function of preweaning calves. J Dairy Sci 93: 5851-5855.
61. Gupta AK, Shashi S, Mohan M, Lamba IM, Gupta R, (1993) Epidemiology of Pseudomonas aeruginosa infections in a neonatal intensive care unit. J Trop Pediatr 39: 32-36.
62. Morowitz MJ, Poroyko V, Caplan M, Alverdy J, Liu DC, (2010) Redefining the role of intestinal microbes in the pathogenesis of necrotizing enterocolitis. Pediatrics 125: 777-785.
63. Inoue T, Shingaki R, Fukui K, (2008) Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett 281: 81-86.
64. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W, (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
65. Rennick DM, Fort MM, (2000) Lessons from genetically engineered animal models. XII. IL-10-deficient (IL-10(-/-) mice and intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 278: G829-G833.
66. Halpern MD, Dominguez JA, Dvorakova K, Holubec H, Williams CS, et al. (2003) Ileal cytokine dysregulation in experimental necrotizing enterocolitis is reduced by epidermal growth factor. J Pediatr Gastroenterol Nutr 36: 126-133.
67. Ozturk H, Dokucu AI, Ogun C, Buyukbayram H, (2002) Protective effects of recombinant human interleukin-10 on intestines of hypoxia-induced necrotizing enterocolitis in immature rats. J Pediatr Surg 37: 1330-1333.
68. Halpern MD, Holubec H, Dominguez JA, Williams CS, Meza YG, et al. (2002) Up-regulation of IL-18 and IL-12 in the ileum of neonatal rats with necrotizing enterocolitis. Pediatr Res 51: 733-739.
69. Sharma R, Tepas JJ, Hudak ML, Mollitt DL, Wludyka PS, et al. (2007) Neonatal gut barrier and multiple organ failure: role of endotoxin and proinflammatory cytokines in sepsis and necrotizing enterocolitis. J Pediatr Surg 42: 454-461.
70. Caplan MS, Sun XM, Hseuh W, Hageman JR, (1990) Role of platelet activating factor and tumor necrosis factor-alpha in neonatal necrotizing enterocolitis. J Pediatr 116: 960-964.
71. Ford H, Watkins S, Reblock K, Rowe M, (1997) The role of inflammatory cytokines and nitric oxide in the pathogenesis of necrotizing enterocolitis. J Pediatr Surg 32: 275-282.
72. Liu Y, Zhu L, Fatheree NY, Liu X, Pacheco SE, et al. (2009) Changes in intestinal Toll-like receptors and cytokines precede histological injury in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 297: G442-G450.