Temporal dynamics of the very premature infant gut dominant microbiota

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Aujoulat, Fabien ^a   Roudière, Laurent ^b   Picaud, Jean Charles ^c   Jacquot, Aurélien ^d   Filleron, Anne ^a,d   Neveu, Dorine ^d   Baum, Thierry Pascal ^d   Marchandin, Hélène ^a,d   Jumas Bilak, Estelle ^a,d  

^a UNIV MONTPELLIER   (France)

^b Centre Hospitalier de Fréjus   (France)

^c HOSPICES CIVILS DE LYON   (France)

^d MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

Clostridium; Diversity; Dynamics; Enterobacteriaceae; Enterococcus; Extremely low birth weight Infant; Follow up; Microbiota; PCR TTGE; Staphylococcus; Stool; Veillonellaceae

Indexed keywords

DNA 16S; BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

ANAEROCOCCUS; AQUABACTERIUM; ARTICLE; BACILLUS; BACTERIA; BACTERIAL COLONIZATION; BIFIDOBACTERIUM; CLOSTRIDIUM; COAGULASE NEGATIVE STAPHYLOCOCCUS; CORYNEBACTERIUM; DYNAMICS; ENTEROBACTERIACEAE; ENTEROCOCCUS; FECES; GENUS; GESTATIONAL AGE; GUT DOMINANT MICROBIOTA; HIGH THROUGHPUT SEQUENCING; HUMAN; INFANT; INTESTINE FLORA; LONGITUDINAL STUDY; MICROCOCCUS; MONITORING; OCEANOBACILLUS; POLYMERASE CHAIN REACTION; PREMATURITY; PROPIONIBACTERIUM; PSEUDOMONAS; ROTHIA; SARCINA; SNEATHIA; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS; VEILLONELLA; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; GASTROINTESTINAL TRACT; GENETICS; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; NEWBORN; PHYLOGENY; TIME FACTOR;

ACIDAMINOCOCCACEAE; ANAEROCOCCUS; AQUABACTERIUM; BIFIDOBACTERIUM; CLOSTRIDIUM; CORYNEBACTERIUM; ENTEROBACTERIACEAE; ENTEROCOCCUS; MICROCOCCUS; OCEANOBACILLUS; OTUS; PROPIONIBACTERIUM; PSEUDOMONAS; ROTHIA; SARCINA; SNEATHIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS; VEILLONELLA;

CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; FECES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; LONGITUDINAL STUDIES; MICROBIOTA; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; TIME FACTORS;

EID: 84923922327     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-014-0325-0     Document Type: Article

References (66)

1. Benno Y, Sawada K, Mitsuoka T: The intestinal microflora of infants: composition of fecal flora in breast-fed and bottle-fed infants. Immunol 1984, 28:975-986.
2. Favier CF, Vaughan EE, de Vos WM, Akkermans DL: Molecular monitoring of succession of bacterial communities in human neonates. Appl Env Microbiol 2002, 68:219-226.
3. 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, 144:186-190.
4. Magne F, Abely M, Boyer F, Morville P, Pochart P, Suau A: Low species diversity and high interindividual variability in faeces of preterm infants as revealed by sequences of 16S rRNA genes and PCR-temporal temperature gradient gel electrophoresis profiles. FEMS Microbiol Ecol 2006, 57:128-138.
5. Chang JY, Shin SM, Chun J, Lee JH, Seo JK: Pyrosequencing-based molecular monitoring of the intestinal bacterial colonization in preterm infants. J Pediatr Gastroenterol Nutr 2011, 53:512-519.
6. Brook I: Microbiology and management of neonatal necrotizing enterocolitis. Am J Perinatol 2008, 25:111-118.
7. Mai V, Torrazza RM, Ukhanova M, Wang X, Sun Y, Li N, Shuster J, Sharma R, Hudak ML, Neu J: Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLoS One 2013, 8:e52876.
8. Claud EC, Walker WA: Bacterial colonization, probiotics, and necrotizing enterocolitis. J Clin Gastroenterol 2008, 42:S46-S52.
9. de la Cochetiere MF, Piloquet H, des Robert C, Darmaun D, Galmiche JP, Roze JC: Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 2004, 56:366-370.
10. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, Neu J: Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 2011, 6:e20647.
11. 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 2007, 369:1614-1620.
12. Butel MJ, Roland N, Hibert A, Popot F, Favre A, Tessedre AC, Bensaada M, Rimbault A, Szylit O: Clostridial pathogenicity in experimental necrotising enterocolitis in gnotobiotic quails and protective role of bifidobacteria. J Med Microbiol 1998, 47:391-399.
13. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO: Development of the human infant intestinal microbiota. PLoS Biol 2007, 5:e177.
14. Gupta S, Morris JG Jr, Panigrahi P, Nataro JP, Glass RI, Gewolb IH: Endemic necrotizing enterocolitis: lack of association with a specific infectious agent. Pediatr Infect Dis J 1994, 13:728-734.
15. Stark PL, Lee A: The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol 1982, 15:189-203.
16. Blakey JL, Lubitz L, Barnes GL, Bishop RF, Campbell NT, Gillam GL: Development of gut colonisation in pre-term neonates. J Med Microbiol 1982, 15:519-529.
17. Rotimi VO, Olowe SA, Ahmed I: The development of bacterial flora of premature neonates. J Hyg (Lond) 1985, 94:309-318.
18. Hall SL, Hall RT, Barnes WG, Riddell SW, Meng L, Parisi JT, Kilbride HW, Maulik D: Relationship of maternal to neonatal colonization with coagulase-negative staphylococci. Am J Perinatol 1990, 7:384-388.
19. Gewolb IH, Schwalbe RS, Taciak VL, Harrison TS, Panigrahi P: Stool microflora in extremely low birthweight infants. Arch Dis Child Fetal Neonatal 1999, 80:F167-F173.
20. Hällström M, Eerola E, Vuento R, Janas M, Tammela O: Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. Eur J Clin Microbiol Infect Dis 2004, 23:463-470.
21. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, Kalach N, Leroux B, Dupont C: Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. J Ped Gastroenterol 2007, 44:577-582.
22. Rougé C, Piloquet H, Butel MJ, Berger B, Rochat F, Ferraris L, Des Robert C, Legrand A, de la Cochetière MF, N'Guyen JM, Vodovar M, Voyer M, Darmaun D, Rozé JC: Oral supplementation with probiotics in very-low-birth-weight preterm infants: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr 2009, 89:1828-1835.
23. Björkström MV, Hall L, Söderlund S, Håkansson EG, Håkansson S, Domellöf M: Intestinal flora in very low-birth weight infants. Acta Paediatr 2009, 98:1762-1767.
24. Roudière L, Jacquot A, Marchandin H, Aujoulat F, Devine R, Zorgniotti I, Jean-Pierre H, Picaud JC, Jumas-Bilak E: Optimized PCR-Temporal Temperature GelElectrophoresis compared to cultivation to assess diversity of gut microbiota in neonates. J Microbiol Methods 2009, 79:156-165.
25. Campeotto F, Suau A, Kapel N, Magne F, Viallon V, Ferraris L, Waligora-Dupriet AJ, Soulaines P, Leroux B, Kalach N, Dupont C, Butel MJ: 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 2011, 22:1-10.
26. Zoetendal EG, Vaughan EE, de Vos WM: A microbial world within us. Mol Microbiol 2006, 59:1639-1650.
27. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, Antonopoulos DA, Chang EB, Claud EC: 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 2009, 3:944-954.
28. Rougé C, Goldenberg O, Ferraris L, Berger B, Rochat F, Legrand A, Göbel UB, Vodovar M, Voyer M, Rozé JC, Darmaun D, Piloquet H, Butel MJ, de La Cochetière MF: Investigation of the intestinal microbiota in preterm infants using different methods. Anaerobe 2010, 16:362-370.
29. Millar MR, Linton CJ, Cade A, Glancy D, Hall M, Jalal H: Application of 16S RNA gene PCR to study bowel flora of preterm infants with and without necroziting enterocolitis. J Clin Microbiol 1996, 34:2506-2510.
30. Schwiertz A, Gruhl B, Löbnitz M, Michel P, Radke M, Blaut M: Development of the intestinal bacterial composition in hospitalized preterm infants in comparison with breast-fed, full-term infants. Pediatr Res 2003, 54:393-399.
31. Mshvildadze M, Neu J, Shuster J, Theriaque D, Li N, Mai V: Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J Pediatr 2010, 156:20-25.
32. Ogier JC, Son O, Gruss A, Tailliez P, Delacroix-Buchet A: Identification of the bacterial microflora in dairy products by temporal temperature gradient gel electrophoresis. Appl Environ Microbiol 2002, 68:3691-3701.
33. Jacquot A, Neveu D, Aujoulat F, Mercier G, Marchandin H, Jumas-Bilak E, Picaud JC: Dynamics and clinical evolution of bacterial gut microflora in extremely premature patients. J Pediatr 2011, 158:390.
34. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, Relman DA, Banfield JF: Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci U S A 2011, 108:1128-1133.
35. LaTuga MS, Ellis JC, Cotton CM, Goldberg RN, Wynn JL, Jackson RB, Seed PC: Beyond bacteria: a study of the enteric microbial consortium in extremely low birth weight infants. PLoS One 2011, 6:e27858.
36. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF: Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 2013, 23(1):111-120.
37. Human Microbiome Project Consortium: Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
38. Ghebremedhin B, Layer F, König W, König B: Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J Clin Microbiol 2008, 46(3):1019-1025.
39. Schleifer KH, MeAyer SA, Rupprecht M: Relatedness among coagulase-negative staphylococci deoxyribonucleic acid reassociation and comparative immunological studies. Arch Microbiol 1979, 122(1):93-101.
40. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA: Diversity of the Human Intestinal Microbial Flora. Science 2005, 308:1635-1638.
41. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, Taylor TD, Noguchi H, Mori H, Ogura Y, Ehrlich DS, Itoh K, Takagi T, Sakaki Y, Hayashi T, Hattori M: Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 2007, 14:169-181.
42. Mackie RI, Sghir A, Gaskins HR: Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999, 69:1035S-1045S.
43. Kafarskaia LI, Volodin NN, Efimov BA, Afanas'ev SS, Shkoporov AN: Peculiarities of microbial colonization of the intestinal tract in newborns and pre-term infants in intensive care units] [Article in Russian. Vestn Ross Akad Med Nauk 2006, 1:10-15.
44. Rønnestad A, Abrahamsen TG, Medbø S, Reigstad H, Lossius K, Kaaresen PI, Engelund IE, Irgens LM, Markestad T: Septicemia in the first week of life in a Norwegian national cohort of extremely premature infants. Pediatrics 2005, 115:e262-e268.
45. Foka A, Chini V, Petinaki E, Kolonitsiou F, Anastassiou ED, Dimitracopoulos G, Spiliopoulou I: Clonality of slime-producing methicillin-resistant coagulase-negative staphylococci disseminated in the neonatal intensive care unit of a university hospital. Clin Microbiol Infect 2006, 12:1230-1233.
46. Soeorg H, Huik K, Parm U, Ilmoja ML, Metelskaja N, Metsvaht T, Lutsar I: Genetic Relatedness of Coagulase-Negative Staphylococci from Gastrointestinal Tract and Blood of Preterm Neonates with Late-Onset Sepsis. Pediatr Infect Dis J 2012, Oct 17. [Epub ahead of print]
47. Jimenez E, Delgado S, Maldonado A, Arroyo R, Albújar M, García N, Jariod M, Fernández L, Gómez A, Rodríguez JM: Staphylococcus epidermidis: a differential trait of the fecal microbiota of breast-fed infants. BMC Microbiol 2008, 10:138-143.
48. Ferraris L, Butel MJ, Campeotto F, Vodovar M, Rozé JC, Aires J: Clostridia in premature neonates' gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization. PLoS One 2012, 7:e30594.
49. Alfa MJ, Robson D, Davi M, Bernard K, Van Caeseele P, Harding GK: An outbreak of necrotizing enterocolitis associated with a novel clostridium species in a neonatal intensive care unit. Clin Infect Dis 2002, 35:S101-S105.
50. Han VK, Dayed H, Chance GW, Brabyn DG, Shaheed WA: An outbreak of Clostridium difficile necrotizing enterocolitis: a case for oral vancomycin therapy? Pediatrics 1983, 71:935-941.
51. Gothefors L, Blenkarn I: Clostridium butyricum and necrotising enterocolitis. Lancet 1978, 1:52-53.
52. Hufnagel M, Liese C, Loescher C, Kunze M, Proempeler H, Berner R, Krueger M: Enterococcal colonization of infants in a neonatal intensive care unit: associated predictors, risk factors and seasonal patterns. BMC Infect Dis 2007, 7:107-128.
53. Rubaltelli FF, Biadaioli R, Pecile P, Nicoletti P: Intestinal flora in breast- and bottle-fed infants. J Perinat Med 1998, 26:186-191.
54. Quintanilha AG, Zilberstein B, Santos MA, Pajecki D, Moura EG, Alves PR, Maluf-Filho F, Cecconello I: A novel sampling method for the investigation of gut mirobiota. World J Gastroenterol 2007, 13:3990-3995.
55. Zilberstein B, Quintanilha AG, Santos MA, Pajecki D, Moura EG, Alves PR, Maluf Filho F, de Souza JA, Gama-Rodrigues J: Digestive tract microbiota in healthy volunteers. Clinics 2007, 62:47-54.
56. Albert MJ, Bhat P, Rajan D, Maiya PP, Pereira SM, Baker SJ: Faecal flora of South Indian infants and young children in health and with acute gastroenteritis. J Med Microbiol 1978, 11:137-143.
57. Malinen E, Rinttilä T, Kajander K, Mättö J, Kassinen A, Krogius L, Saarela M, Korpela R, Palva A: Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 2005, 100:373-382.
58. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW: Analysis of intestinal flora development in breastfed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 2000, 30:61-67.
59. Rotimi VO, Duerden BI: The development of the bacterial flora in normal neonates. J Med Microbiol 1981, 14:51-62.
60. Könönen E, Kanervo A, Takala A, Asikainen S, Jousimies-Somer H: Establishment of oral anaerobes during the first year of life. J Dent Res 1999, 78:1634-1639.
61. Egland PG, Palmer RJ Jr, Kolenbrander PE: Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc Natl Acad Sci U S A 2004, 101:16917-16922.
62. Kumar PS, Leys EJ, Bryk JM, Martinez FJ, Moeschberger ML, Griffen AL: Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 2006, 44:3665-3673.
63. Diaz PI, Chalmers NI, Rickard AH, Kong C, Milburn CL, Palmer RJ Jr, Kolenbrander PE: Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol 2006, 72:2837-2848.
64. Park HK, Shim SS, Kim SY, Park JH, Park SE, Kim HJ, Kang BC, Kim CM: Molecular analysis of colonized bacteria in a human newborn infant gut. J Microbiol 2005, 43:345-353.
65. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O'Toole PW, van Sinderen D, Marchesi JR, Ventura M: Diversity of bifidobacteria within the infant gut microbiota. PLoS One 2012, 7:e36957.
66. Lin HC, Hsu CH, Chen HL, Chung MY, Hsu JF, Lien RI, Tsao LY, Chen CH, Su BH: Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics 2008, 122: 693-700.