The Altered Gut Microbiome and Necrotizing Enterocolitis

Clinics in Perinatology

Volumn 40, Issue 1, 2013, Pages 93-108

  Torrazza, Roberto Murgas ^a   Neu, Josef ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Intestinal microbiota; Microbiome; Necrotizing enterocolitis; Noncultured based techniques; Sequencing

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; ENDOTHELIN 1; GENTAMICIN; HISTAMINE H2 RECEPTOR AGONIST; INTERFERON; INTERLEUKIN 1; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; PROBIOTIC AGENT; RNA 16S; THROMBOCYTE ACTIVATING FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANTIBIOTIC THERAPY; ARTIFICIAL MILK; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL TRANSLOCATION; BACTERIUM CULTURE; BREAST MILK; CESAREAN SECTION; CYTOKINE RESPONSE; FECES ANALYSIS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE DYSREGULATION; INFANT FEEDING; INFECTION RISK; INFECTION SENSITIVITY; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE FUNCTION DISORDER; MENINGITIS; MICROBIAL DIVERSITY; NECROTIZING ENTEROCOLITIS; NEWBORN INFECTION; NEWBORN INTENSIVE CARE; NONHUMAN; PATHOGENESIS; PERINATAL PERIOD; POLYMERASE CHAIN REACTION; PREMATURITY; PRENATAL PERIOD; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SEPSIS; STOMACH PH; VAGINAL DELIVERY;

ANTI-BACTERIAL AGENTS; ENTEROCOLITIS, NECROTIZING; GENETIC TECHNIQUES; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; INTESTINES; METAGENOME;

EID: 84873721305     PISSN: 00955108     EISSN: 15579840     Source Type: Journal    
DOI: 10.1016/j.clp.2012.12.009     Document Type: Review

References (77)

1. Obladen M. Necrotizing enterocolitis-150 years of fruitless search for the cause. Neonatology 2009, 96(4):203-210.
2. Neu J., Walker W.A. Necrotizing enterocolitis. N Engl J Med 2011, 364(3):255-264.
3. Lin Patricia W., Stoll Barbara J. Necrotising enterocolitis. Lancet 2006, 368(9543):1271-1283.
4. Young C.M., Kingma S.D., Neu J. Ischemia-reperfusion and neonatal intestinal injury. J Pediatr 2011, 158(2 Suppl):e25-e28.
5. Claud E.C., Walker W.A. Hypothesis: inappropriate colonization of the premature intestine can cause neonatal necrotizing enterocolitis. FASEB J 2001, 15(8):1398-1403.
6. Sántulli T.V., Schullinger J.N., Heird W.C., et al. Acute necrotizing enterocolitis in infancy: a review of 64 cases. Pediatrics 1975, 55(3):376-387.
7. Falkow S. Molecular Koch's postulates applied to bacterial pathogenicity-a personal recollection 15 years later. Nat Rev Microbiol 2004, 2(1):67-72.
8. Resta S., Luby J.P., Rosenfeld C.R., et al. Isolation and propagation of a human enteric coronavirus. Science 1985, 229(4717):978-981.
9. Neu J., Mshvildadze M., Mai V. A roadmap for understanding and preventing necrotizing enterocolitis. Curr Gastroenterol Rep 2008, 10(5):450-457.
10. Grave G.D., Nelson S.A., Walker W.A., et al. New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr Res 2007, 62(4):510-514.
11. Ben-Amor K., Heilig H., Smidt H., et al. Genetic diversity of viable, injured, and dead fecal bacteria assessed by fluorescence-activated cell sorting and 16S rRNA gene analysis. Appl Environ Microbiol 2005, 71(8):4679-4689.
12. Leblond-Bourget N., Philippe H., Mangin I., et al. 16S rRNA and 16S to 23S internal transcribed spacer sequence analyses reveal inter- and intraspecific Bifidobacterium phylogeny. Int J Syst Bacteriol 1996, 46(1):102-111.
13. Rondon M.R., August P.R., Bettermann A.D., et al. Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 2000, 66(6):2541-2547.
14. Venter J.C., Remington K., Heidelberg J.F., et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304(5667):66-74.
15. Turnbaugh P.J., Quince C., Faith J.J., et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci U S A 2010, 107(16):7503-7508.
16. Gosalbes M.J., Durban A., Pignatelli M., et al. Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 2011, 6(3):e17447.
17. Zoetendal E.G., Raes J., van den Bogert B., et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 2012, 6(7):1415-1426.
18. Booijink C.C., Boekhorst J., Zoetendal E.G., et al. Metatranscriptome analysis of the human fecal microbiota reveals subject-specific expression profiles, with genes encoding proteins involved in carbohydrate metabolism being dominantly expressed. Appl Environ Microbiol 2010, 76(16):5533-5540.
19. Verberkmoes N.C., Russell A.L., Shah M., et al. Shotgun metaproteomics of the human distal gut microbiota. ISME J 2009, 3(2):179-189.
20. Hooper L.V., Gordon J.I. Commensal host-bacterial relationships in the gut. Science 2001, 292(5519):1115-1118.
21. Forsythe P., Bienenstock J. Immunomodulation by commensal and probiotic bacteria. Immunol Invest 2010, 39(4-5):429-448.
22. Wang Y., Hoenig J.D., Malin K.J., et al. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 2009, 3(8):944-954.
23. Mai V., Young C.M., Ukhanova M., et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 2011, 6(6):e20647.
24. DiGiulio D.B., Gervasi M.T., Romero R., et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J Perinat Med 2010, 38(5):495-502.
25. Nanthakumar N.N., Fusunyan R.D., Sanderson I., et al. Inflammation in the developing human intestine: a possible pathophysiologic contribution to necrotizing enterocolitis. Proc Natl Acad Sci U S A 2000, 97(11):6043-6048.
26. Medzhitov R., Schneider D.S., Soares M.P. Disease tolerance as a defense strategy. Science 2012, 335(6071):936-941.
27. Harmsen H.J., Wildeboer-Veloo A.C., Raangs G.C., et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 2000, 30(1):61-67.
28. Jernberg C., Lofmark S., Edlund C., et al. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 2007, 1(1):56-66.
29. Gronlund M.M., Lehtonen O.P., Eerola E., et al. Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999, 28(1):19-25.
30. Neu J., Rushing J. Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis. Clin Perinatol 2011, 38(2):321-331.
31. Dominguez-Bello M.G., Blaser M.J., Ley R.E., et al. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology 2011, 140(6):1713-1719.
32. Dominguez-Bello M.G., Costello E.K., Contreras M., et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A 2010, 107(26):11971-11975.
33. Sullivan S., Schanler R.J., Kim J.H., et al. An exclusively human milk-based diet is associated with a lower rate of necrotizing enterocolitis than a diet of human milk and bovine milk-based products. J Pediatr 2010, 156(4):562-567.e1.
34. Barlow B., Santulli T.V., Heird W.C., et al. An experimental study of acute neonatal enterocolitis-the importance of breast milk. J Pediatr Surg 1974, 9(5):587-595.
35. Lucas A., Cole T.J. Breast milk and neonatal necrotising enterocolitis. Lancet 1990, 336(8730):1519-1523.
36. Hanson L.A., Korotkova M., Telemo E. Breast-feeding, infant formulas, and the immune system. Ann Allergy Asthma Immunol 2003, 90(6 Suppl 3):59-63.
37. Ward R.E., Ninonuevo M., Mills D.A., et al. In vitro fermentation of breast milk oligosaccharides by Bifidobacterium infantis and Lactobacillus gasseri. Appl Environ Microbiol 2006, 72(6):4497-4499.
38. Ninonuevo M.R., Park Y., Yin H., et al. A strategy for annotating the human milk glycome. J Agric Food Chem 2006, 54(20):7471-7480.
39. Adlerberth I., Lindberg E., Aberg N., et al. Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle?. Pediatr Res 2006, 59(1):96-101.
40. Bjorkstrom M.V., Hall L., Soderlund S., et al. Intestinal flora in very low-birth weight infants. Acta Paediatr 2009, 98(11):1762-1767.
41. Le Huerou-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.
42. Penders J., Thijs C., Vink C., et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006, 118(2):511-521.
43. Section on Breastfeeding Breastfeeding and the use of human milk. Pediatrics 2012, 129(3):e827-e841.
44. Kuppala V.S., Meinzen-Derr J., Morrow A.L., et al. Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. J Pediatr 2011, 159(5):720-725.
45. Alexander V.N., Northrup V., Bizzarro M.J. Antibiotic exposure in the newborn intensive care unit and the risk of necrotizing enterocolitis. J Pediatr 2011, 159(3):392-397.
46. Weintraub A.S., Ferrara L., Deluca L., et al. Antenatal antibiotic exposure in preterm infants with necrotizing enterocolitis. J Perinatol 2012, 32(9):705-709.
47. Goldmann D.A., Leclair J., Macone A. Bacterial colonization of neonates admitted to an intensive care environment. J Pediatr 1978, 93(2):288-293.
48. Jakobsson H.E., Jernberg C., Andersson A.F., et al. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 2010, 5(3):e9836.
49. Cotten C.M., Taylor S., Stoll B., et al. Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics 2009, 123(1):58-66.
50. Caplan M.S., MacKendrick W. Necrotizing enterocolitis: a review of pathogenetic mechanisms and implications for prevention. Pediatr Pathol 1993, 13(3):357-369.
51. Caplan M.S., Sun X.M., Hseuh W., et al. Role of platelet activating factor and tumor necrosis factor-alpha in neonatal necrotizing enterocolitis. J Pediatr 1990, 116(6):960-964.
52. Edelson M.B., Bagwell C.E., Rozycki H.J. Circulating pro- and counterinflammatory cytokine levels and severity in necrotizing enterocolitis. Pediatrics 1999, 103(4 Pt 1):766-771.
53. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009, 9(5):313-323.
54. Murgas Torrazza R., Neu J. The developing intestinal microbiome and its relationship to health and disease in the neonate. J Perinatol 2011, 31(Suppl 1):S29-S34.
55. Rook G.A. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Darwinian medicine and the 'hygiene' or 'old friends' hypothesis. Clin Exp Immunol 2010, 160(1):70-79.
56. Macpherson A.J., Harris N.L. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004, 4(6):478-485.
57. Coats S.R., Do C.T., Karimi-Naser L.M., et al. Antagonistic lipopolysaccharides block E. coli lipopolysaccharide function at human TLR4 via interaction with the human MD-2 lipopolysaccharide binding site. Cell Microbiol 2007, 9(5):1191-1202.
58. Sansonetti P.J., Medzhitov R. Learning tolerance while fighting ignorance. Cell 2009, 138(3):416-420.
59. Munford R.S., Varley A.W. Shield as signal: lipopolysaccharides and the evolution of immunity to gram-negative bacteria. PLoS Pathog 2006, 2(6):e67.
60. Sharma R., Young C., Neu J. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J Biomed Biotechnol 2010, 2010:305879.
61. Rhee S.H. Basic and translational understandings of microbial recognition by toll-like receptors in the intestine. J Neurogastroenterol Motil 2011, 17(1):28-34.
62. Caplan M.S. Probiotic and prebiotic supplementation for the prevention of neonatal necrotizing enterocolitis. J Perinatol 2009, 29(Suppl 2):S2-S6.
63. Tien M.T., Girardin S.E., Regnault B., et al. Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 2006, 176(2):1228-1237.
64. Otte J.M., Podolsky D.K. Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am J Physiol Gastrointest Liver Physiol 2004, 286(4):G613-G626.
65. Lin H.C., Hsu C.H., Chen H.L., et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 2008, 122(4):693-700.
66. Deshpande G., Rao S., Patole S., et al. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 2010, 125(5):921-930.
67. Floch M.H., Walker W.A., Madsen K., et al. Recommendations for probiotic use-2011 update. J Clin Gastroenterol 2011, 45(Suppl):S168-S171.
68. Zhang L., Li N., Caicedo R., et al. Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 2005, 135(7):1752-1756.
69. Zhang L., Li N., des Robert C., et al. Lactobacillus rhamnosus GG decreases lipopolysaccharide-induced systemic inflammation in a gastrostomy-fed infant rat model. J Pediatr Gastroenterol Nutr 2006, 42(5):545-552.
70. Sherman M.P. New concepts of microbial translocation in the neonatal intestine: mechanisms and prevention. Clin Perinatol 2010, 37(3):565-579.
71. Hunter C.J., Upperman J.S., Ford H.R., et al. Understanding the susceptibility of the premature infant to necrotizing enterocolitis (NEC). Pediatr Res 2008, 63(2):117-123.
72. Gatt M., Reddy B.S., MacFie J. Review article: bacterial translocation in the critically ill-evidence and methods of prevention. Aliment Pharmacol Ther 2007, 25(7):741-757.
73. Anand R.J., Leaphart C.L., Mollen K.P., et al. The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock 2007, 27(2):124-133.
74. Cole C.R., Hansen N.I., Higgins R.D., et al. Bloodstream infections in very low birth weight infants with intestinal failure. J Pediatr 2012, 160(1):54-59.e2.
75. Guillet R., Stoll B.J., Cotten C.M., et al. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006, 117(2):e137-e142.
76. Canani R.B., Terrin G. Gastric acidity inhibitors and the risk of intestinal infections. Curr Opin Gastroenterol 2010, 26(1):31-35.
77. Carrion V., Egan E.A. Prevention of neonatal necrotizing enterocolitis. J Pediatr Gastroenterol Nutr 1990, 11(3):317-323.