Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: A case-control study

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Zhou, Yanjiao ^a   Shan, Gururaj ^b   Sodergren, Erica ^c   Weinstock, George ^c   Walker, W Allan ^d,f   Gregory, Katherine E ^e,f  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Pediatrics Washington University School of Medicine ^*  (United States)

^c JACKSON LABORATORY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APGAR SCORE; ARTICLE; CASE CONTROL STUDY; CLINICAL ARTICLE; CLOSTRIDIUM; CONTROLLED STUDY; CRONOBACTER; ESCHERICHIA COLI; FEMALE; GEL ELECTROPHORESIS; HUMAN; IMMUNOREGULATION; INFANT; LONGITUDINAL STUDY; MALE; MICROBIAL COLONIZATION; MICROBIOME; MICROFLORA; NECROTIZING ENTEROCOLITIS; POLYMERASE CHAIN REACTION; PROSPECTIVE STUDY; SEX DIFFERENCE; SHIGELLA; FECES; INTESTINE; INTESTINE FLORA; MICROBIOLOGY; NEWBORN; PREMATURITY;

CLOSTRIDIA; CLOSTRIDIUM; GAMMAPROTEOBACTERIA;

RNA 16S;

CASE-CONTROL STUDIES; ENTEROCOLITIS, NECROTIZING; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; INTESTINES; LONGITUDINAL STUDIES; MALE; RNA, RIBOSOMAL, 16S;

EID: 84924288745     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118632     Document Type: Article

References (42)

1. Costello EK, Carlisle EM, Bik EM, Morowitz MJ, Relman DA. Micro biome assembly across multiple body sites in low-birth weight infants. MBio. 2013; 4: e00782-e00713. doi:10.1128/mBio.00782-13 PMID: 24169577.
2. Madan JC, Salari RC, Saxena D, Davidson L, O'Toole GA, Moore JH, et al. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed. 2012; 97: F456-F462. doi:10.1136/fetalneonatal-2011-301373 PMID: 22562869.
3. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, Relman DA, et al. Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci U S A. 2011; 108: 1128-1133. doi:10.1073/pnas.1010992108 PMID: 21191099.
4. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF, et al. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res. 2013; 23: 111-120. doi:10.1101/gr.142315.112 PMID: 22936250.
5. Nanthakumar NN, Fusunyan RD, Sanderson I, Walker WA. Inflammation in the developing human intestine: A possible pathophysiologic contribution to necrotizing enterocolitis. Proc Natl Acad Sci U S A. 2000; 97: 6043-6048. PMID: 10823949.
6. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011; 364: 255-264. doi:10.1056/NEJMra1005408PMID: 21247316.
7. Wadhawan R, OhW, Hintz SR, Blakely ML, Das A, Bell EF, et al. Neuro developmental outcomes of extremely low birth weight infants with spontaneous intestinal perforation or surgical necrotizing enterocolitis. J Perinatol. 2014; 34: 64-70. doi:10.1038/jp.2013.128 PMID: 24135709.
8. Holman RC, Stoll BJ, Curns AT, Yorita KL, Steiner CA, Schonberger LB, et al. Necrotising enterocolitis hospitalisations among neonates in the United States. Paediatr Perinat Epidemiol. 2006; 20: 498-506. PMID: 17052286.
9. Stoll BJ, Hansen NI, Bell EF, Shankaran S, Laptook AR, Walsh MC, et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics. 2010; 126: 443-456. doi:10.1542/peds.2009-2959 PMID: 20732945.
10. Normann E, Fahlen A, Engstrand L, Lilja HE. Intestinal microbial profiles in extremely preterm infants with and without necrotizing enterocolitis. Acta Paediatr. 2013; 102: 129-136. doi:10.1111/apa.12059 PMID: 23082780.
11. Mshvildadze M, Neu J, Shuster J, Theriaque D, Li N, Mai V, et al. Intestinal microbial ecology in premature infants assessed with non-culture-based techniques. J Pediatr. 2010; 156: 20-25. doi:10.1016/j.jpeds.2009.06.063 PMID: 19783002.
12. Claud EC, Keegan KP, Brulc JM, Lu L, Bartels D, Glass E, et al. Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Micro biome. 2013; 1: 20. doi:10.1186/2049-2618-1-20 PMID: 24450928.
13. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, et al. 16S rRNA gene-based analysis of fecal micro biota from preterm infants with and without necrotizing enterocolitis. ISME. 2009; 3: 944-954. doi:10.1038/ismej.2009.37 PMID: 19369970.
14. Torrazza RM, Ukhanova M, Wang X, Sharma R, Hudak ML, Neu J, et al. Intestinal microbial ecology and environmental factors affecting necrotizing enterocolitis. PLoS One. 2013; 8: e83304. doi:10.1371/journal.pone.0083304 PMID: 24386174.
15. Morrow AL, Lagomarcino AJ, Schibler KR, Taft DH, Yu Z, Wang B, et al. Early microbial and meta bolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Micro biome. 2013; 1: 13. doi:10.1186/2049-2618-1-13 PMID: 24450576.
16. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, et al. Fecal micro biota in premature infants prior to necrotizing enterocolitis. PLoS One. 2011; 6: e20647. doi:10.1371/journal.pone.0020647PMID: 21674011.
17. Walsh MC, Kliegman RM. Necrotizing enterocolitis: Treatment based on staging criteria. Pediatr Clin North Am. 1986; 33: 179-201. PMID: 3081865.
18. Gordon PV, Swanson JR, Attridge JT, Clark R. Emerging trends in acquired neonatal intestinal disease: Is it time to abandon Bell's criteria? J Perinatol. 2007; 27: 661-671. PMID: 17611610.
19. The Human Micro biome Consortium. A framework for human microbiome research. Nature. 2012; 486: 215-221. doi:10.1038/nature11209 PMID: 22699610.
20. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 2011; 21: 494-504. doi: 10.1101/gr.112730.110 PMID: 21212162.
21. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. Vegan: Community Ecology Package. R package version 2.0-7. Available: http://cranr-projectorg/package=vegan (2013).
22. White JR, Nagarajan N, Pop M. Statistical methods for detection differentially abundant features in clinical meta genomic samples. PLoS Computational Biology. 2009; 5: e1000352. doi:10.1371/journal.pcbi.1000352 PMID: 19360128.
23. Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T, et al. Biogeography of the ecosystems of the healthy human body. Genome Biol. 2013; 14: R1. doi:10.1186/gb-2013-14-1-r1 PMID: 23316946.
24. Bates D, Maechler M, Bolker B. lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0. Available: http://Cran.r-project.org/package=lme4 (2012).
25. Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, et al. (The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol. 1994; 44: 812-826. PMID: 7981107.
26. Perez-Cobas AE, Gosalbes MJ, Friedrichs A, Knecht H, Artacho A, Eismann K, et al. Gut micro biota disturbance during antibiotic therapy: A multi-omic approach. Gut. 2013; 62: 1591-1601. doi:10.1136/gutjnl-2012-303184PMID: 23236009.
27. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut micro biome viewed across age and geography. Nature. 2012; 486: 222-227. doi:10.1038/nature11053 PMID: 22699611.
28. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal micro biota. PLoS Biol. 2007; 5: e177. PMID: 17594176.
29. LaRosa P, Warner B, Zhou Y, Weinstock G, Sodergren E, Hall-Moore CM, et al. The Patterned Progression of Bacterial Populations in the Premature Infant Gut. Proc Natl Acad Sci U S A. 2014; 111: 12522-12527. doi:10.1073/pnas.1409497111 PMID: 25114261.
30. Grishin A, Papillon S, Bell B, Wang J, Ford HR. The role of the intestinal micro biota in the pathogenesis of necrotizing enterocolitis. Semin Pediatr Surg. 2013; 22: 69-75. doi:10.1053/j.sempedsurg.2013.01.002 PMID: 23611609.
31. Hunter CJ, Singamsetty VK, Chokshi NK, Boyle P, Camerini V, Grishin AV, et al. Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J Infect Dis. 2008; 198: 586-593. doi: 10.1086/590186 PMID: 18588483.
32. Emami CN, Mittal R, Wang L, Ford HR, Prasadarao NV. Role of neutrophils and macrophages in the pathogenesis of necrotizing enterocolitis caused by Cronobacter sakazakii. J Surg Res. 2012; 172: 18-28. doi:10.1016/j.jss.2011.04.019 PMID: 21601887.
33. Weng M, Ganguli K, Zhu W, Shi HN, Walker WA. Conditioned medium from Bifidobacteria infantis protects against Cronobacter sakazakii-induced intestinal inflammation in newborn mice. Am J Physiol Gastrointest Liver Physiol. 2014; 306: G779-G787. doi:10.1152/ajpgi.00183.2013 PMID: 24627567.
34. Jenke AC, Postberg J, Mariel B, Hensel K, Foell D, Däbritz J, et al. S100A12 and hBD2 correlate with the composition of the fecal micro flora in ELBW infants and expansion of E. coli is associated with NEC. Biomed Res Int. 2013; 150372. doi:10.1155/2013/150372 PMID: 24307989.
35. Mai V, Torrazza RM, Ukhanova M, Wang X, Sun Y, Li N, et al. Distortions in development of intestinal micro biota associated with late onset sepsis in preterm infants. PLoS One. 2013; 8: e52876. doi:10.1371/journal.pone.0052876 PMID: 23341915.
36. Hallstrom M, Eerola E, Vuento R, Janas M, Tammela O. Effects of mode of delivery and necrotising enterocolitis on the intestinal micro flora in preterm infants. Eur J Clin Microbiol Infect Dis. 2004; 23: 463-470. PMID: 15168141.
37. de la Cochetiere MF, Piloquet H, des Robert C, Darmaun D, Galmiche JP, Roze JC, et al. (Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: The putative role of Clostridium. Pediatr Res. 2004; 56: 366-370. PMID: 15201403.
38. Elahi S, Ertelt JM, Kinder JM, Jiang TT, Zhang X, Xin L, et al. Immunosuppressive CD71+ erythroid cells compromise neonatal host defence against infection. Nature. 2013; 504: 158-162. doi:10.1038/nature12675 PMID: 24196717.
39. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, et al. Conducting a micro biome study. Cell. 2014; 158: 250-262. doi:10.1016/j.cell.2014.06.037 PMID: 25036628.
40. Sullivan S, Schanler RJ, Kim JH, Patel AL, Trawoger R, Kiechl-Kohlendorfer U, 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: 562-567.e561. doi:10.1016/j.jpeds.2009.10.040 PMID: 20036378.
41. Ardeshir A, Narayan NR, Méndez-Lagares G, Lu D, Rauch M, Huang Y, et al. Breast-fed and bottle-fed infant rhesus macaques develop distinct gut micro biotas and immune systems. Science Translational Medicine. 2014; 6: 252ra120. doi:10.1126/scitranslmed.3008791 PMID: 25186175.
42. O'Sullivan A, He X, McNiven EM, Haggarty NW, Lonnerdal B, Slupsky CM, et al. Early diet impacts infant rhesus gut micro biome, immunity, and metabolism. J Proteome Res. 2013; 12: 2833-2845. doi:10.1021/pr4001702 PMID: 23651394.