Nutritional strategies and gut microbiota composition as risk factors for necrotizing enterocolitis in very-preterm infants

American Journal of Clinical Nutrition

Volumn 106, Issue 3, 2017, Pages 821-830

  Rozé, Jean Christophe ^a,b   Ancel, Pierre Yves ^c,d,e   Lepage, Patricia ^f   Martin Marchand, Laetitia ^c   Nabhani, Ziad Al ^f   Delannoy, Johanne ^d   Picaud, Jean Charles ^g   Lapillonne, Alexandre ^h   Aires, Julio ^d   Durox, Mélanie ^c   Darmaun, Dominique ^b   Neu, Josef ⁱ   Butel, Marie José ^d   Boudred, Farid ^j   Mitanchez, Delphine ^k   Casper, Charlotte ^l   Biran, Valérie ^d   Storme, Laurent ^m   Claris, Olivier ⁿ   Cambonie, Gilles ^o   Sizun, Jacques ^p   Sauret, Anne ^q   Dicky, Odile ^l   Lopez, Emmanuel ^r   Hascoet, Jean Michel ^s   Gascoin, Geraldine ^t   Vieux, Rachel ^u   De Lauzon, Blandine ^c   Desfrère, Luc ^v   Chollat, Clement ^w   Doré, Joel ^x   Le Roux, Karine ^x   Monot, Céline ^x   Rousseau, Clotilde ^d   more..

^a NANTES UNIVERSITY HOSPITAL   (France)

^b Universite de Nantes   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔTEL DIEU   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

^g CROIX ROUSSE HOSPITAL   (France)

^h HÔPITAL NECKER ENFANTS MALADES   (France)

ⁱ UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^j AIX MARSEILLE UNIVERSITY   (France)

^k ARMAND TROUSSEAU HOSPITAL   (France)

^l TOULOUSE UNIVERSITY HOSPITAL   (France)

^m LILLE UNIVERSITY HOSPITAL   (France)

ⁿ Department of Paediatric Surgery   (France)

^o MONTPELLIER UNIVERSITY HOSPITAL   (France)

^p BREST UNIVERSITY HOSPITAL   (France)

^q RENNES UNIVERSITY HOSPITAL   (France)

^r UNIVERSITÉ DE TOURS   (France)

^s UNIVERSITY HOSPITAL OF NANCY   (France)

^t ANGERS UNIVERSITY HOSPITAL   (France)

^u UNIVERSITY HOSPITAL OF BESANÇON   (France)

^v HÔPITAL LOUIS MOURIER   (France)

^w Institut Cochin   (France)

^x UMR1319 MICALIS   (France)

more..

Author keywords

Breastfeeding; Clostridia; Necrotizing enterocolitis; Preterm infant; Speed of increasing enteral nutrition

Indexed keywords

APGAR SCORE; ARTICLE; BIRTH WEIGHT; BREAST FEEDING; CASE CONTROL STUDY; CLOSTRIDIUM; CLOSTRIDIUM NEONATALE; COHORT ANALYSIS; ENTERIC FEEDING; FEMALE; GESTATIONAL AGE; HUMAN; INTESTINE FLORA; MAJOR CLINICAL STUDY; MALE; NECROTIZING ENTEROCOLITIS; NEONATAL INTENSIVE CARE UNIT; NUTRITIONAL STATUS; OUTCOME ASSESSMENT; PREMATURITY; PROSPECTIVE STUDY; RISK FACTOR; STAPHYLOCOCCUS AUREUS; ARTIFICIAL MILK; BACTERIUM; BREAST MILK; ENTEROCOLITIS, NECROTIZING; FRANCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; NEWBORN; NEWBORN INTENSIVE CARE; ODDS RATIO; PROCEDURES; TIME FACTOR;

RNA 16S;

BACTERIA; BREAST FEEDING; CASE-CONTROL STUDIES; CLOSTRIDIUM; ENTERAL NUTRITION; ENTEROCOLITIS, NECROTIZING; FRANCE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT FORMULA; INFANT, NEWBORN; INFANT, PREMATURE; INTENSIVE CARE UNITS, NEONATAL; INTENSIVE CARE, NEONATAL; MILK, HUMAN; ODDS RATIO; PROSPECTIVE STUDIES; RISK FACTORS; RNA, RIBOSOMAL, 16S; STAPHYLOCOCCUS AUREUS; TIME FACTORS;

EID: 85028734458     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.117.152967     Document Type: Article

References (50)

1. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med 2011;364:255-64.
2. Lin PW, Stoll BJ. Necrotising enterocolitis. Lancet 2006;368:1271-83.
3. Neu J. Necrotizing enterocolitis: the mystery goes on. Neonatology 2014;106:289-95.
4. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev 2014;4: CD005496.
5. 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;369:1614-20.
6. Costeloe K, Hardy P, Juszczak E, Wilks M, Millar MR. Bifidobacterium breve BBG-001 in very preterm infants: a randomised controlled phase 3 trial. Lancet 2016;387:649-60.
7. Quigley M, McGuire W. Formula versus donor breast milk for feeding preterm or low birth weight infants. Cochrane Database Syst Rev 2014; 4:CD002971.
8. Talavera MM, Bixler G, Cozzi C, Dail J, Miller RR, McClead R Jr., Reber K. Quality improvement initiative to reduce the necrotizing enterocolitis rate in premature infants. Pediatrics 2016;137:e20151119.
9. 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;3:944-54.
10. Mai V, Young CM, Ukhanova M, Wang X, Sun Y, Casella G, Theriaque D, Li N, Sharma R, Hudak M, et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS One 2011;6:e20647.
11. Torrazza RM, Ukhanova M, Wang X, Sharma R, Hudak ML, Neu J, Mai V. Intestinal microbial ecology and environmental factors affecting necrotizing enterocolitis. PLoS One 2013;8:e83304.
12. Morrow AL, Lagomarcino AJ, Schibler KR, Taft DH, Yu Z, Wang B, Altaye M, Wagner M, Gevers D, Ward DV, et al. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 2013;1:13-.
13. Morowitz MJ, Poroyko V, Caplan M, Alverdy J, Liu DC. Redefining the role of intestinal microbes in the pathogenesis of necrotizing enterocolitis. Pediatrics 2010;125:777-85.
14. Warner BB, Deych E, Zhou Y, Hall-Moore C, Weinstock GM, Sodergren E, Shaikh N, Hoffmann JA, Linneman LA, Hamvas A, et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Lancet 2016;387:1928-36.
15. 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;158:390-6.
16. Claud EC, Keegan KP, Brulc JM, Lu L, Bartels D, Glass E, Chang EB, Meyer F, Antonopoulos DA. Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Microbiome 2013;1:20-.
17. Smith B, Bode S, Petersen BL, Jensen TK, Pipper C, Kloppenborg J, Boye M, Krogfelt KA, Molbak L. Community analysis of bacteria colonizing intestinal tissue of neonates with necrotizing enterocolitis. BMC Microbiol 2011;11:73.
18. 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:S101-5.
19. Cassir N, Benamar S, Khalil JB, Croce O, Saint-Faust M, Jacquot A, Million M, Azza S, Armstrong N, Henry M, et al. Clostridium butyricum strains and dysbiosis linked to necrotizing enterocolitis in preterm neonates. Clin Infect Dis 2015;61:1107-15.
20. Sim K, Shaw AG, Randell P, Cox MJ, McClure ZE, Li MS, Haddad M, Langford PR, Cookson WO, Moffatt MF, et al. Dysbiosis anticipating necrotizing enterocolitis in very premature infants. Clin Infect Dis 2015;60:389-97.
21. de la Cochetie're MF, Piloquet H, Des Robert C, Darmaun D, Galmiche JP, Rozé JC. Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of clostridium. Pediatr Res 2004;56:366-70.
22. Zhou Y, Shan G, Sodergren E, Weinstock G, Walker WA, Gregory KE. Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study. PLoS One 2015; 10:e0118632.
23. Heida FH, van Zoonen AG, Hulscher JB, Te Kiefte BJ, Wessels R, Kooi EM, Bos AF, Harmsen HJ, de Goffau MC. A necrotizing enterocolitis-associated gut microbiota is present in the meconium: results of a prospective study. Clin Infect Dis 2016;62:863-70.
24. Ancel PY, Goffinet F, Kuhn P, Langer B, Matis J, Hernandorena X, Chabanier P, Joly-Pedespan L, Lecomte B, Vendittelli F, et al.; EPIPAGE 2 Writing Group. Survival and morbidity of preterm children born at 22 through 34 weeks' gestation in France in 2011: results of the EPIPAGE-2 cohort study. JAMA Pediatr 2015;169:230-8.
25. Erratum in: JAMA Pediatr 2015;169:323.
26. Waligora-Dupriet AJ, Dugay A, Auzeil N, Huerre M, Butel MJ. Evidence for clostridial implication in necrotizing enterocolitis through bacterial fermentation in a gnotobiotic quail model. Pediatr Res 2005; 58:629-35.
27. Walsh MC, Kliegman RM. Necrotizing enterocolitis: treatment based on staging criteria. Pediatr Clin North Am 1986;33:179-201.
28. Suply E, Leclair MD, Neunlist M, Roze JC, Flamant C. Spontaneous intestinal perforation and necrotizing enterocolitis: a 16-year retrospective study from a single center. Eur J Pediatr Surg 2015;25:520-5.
29. Gordon PV, Attridge JT. Understanding clinical literature relevant to spontaneous intestinal perforations. Am J Perinatol 2009;26:309-16.
30. Olsen IE. Groveman SA, Lawson ML, Clark RH, Zemel BS. New intrauterine growth curves based on United States data. Pediatrics 2010;125: e214-24.
31. Durrmeyer X, Marchand-Martin L, Porcher R, Gascoin G, Roze JC, Storme L, Favrais G, Ancel PY, Cambonie G; Hemodynamic EPIPAGE 2 Study Group. Abstention or intervention for isolated hypotension in the first 3 days of life in extremely preterm infants: association with short-term outcomes in the EPIPAGE 2 cohort study. Arch Dis Child Fetal Neonatal Ed 2017 Mar 16 (Epub ahead of print; DOI: 10.1136/ archdischild-2016-312104).
32. Weaver LT, Lucas O. Development of bowel habit in preterm infants. Arch Dis Child 1993;68:317-20.
33. Rougé C, Goldenberg O, Ferraris L, Berger B, Rochat F, Legrand A, Gobel UB, Vodovar M, Voyer M, Roze JC, et al. Investigation of the intestinal microbiota in preterm infants using different methods. Anaerobe 2010;16:362-70.
34. Crissinger KD. Regulation of hemodynamics and oxygenation in developing intestine: insight into the pathogenesis of necrotizing enterocolitis. Acta Paediatr Suppl 1994;396:8-10.
35. Young CM, Kingma SD, Neu J. Ischemia-reperfusion and neonatal intestinal injury. J Pediatr 2011;158:e25-8.
36. Michel F, Vialet R, Hassid S, Nicaise C, Garbi A, Thomachot LDI, Marco JN, Lagier P, Martin C. Sevoflurane for central catheter placement in neonatal intensive care: a randomized trial. Paediatr Anaesth 2010;20:712-9.
37. Morgan J, Young L, McGuire W. Delayed introduction of progressive enteral feeds to prevent necrotising enterocolitis in very low birth weight infants. Cochrane Database Syst Rev 2014;12:CD001970.
38. Morgan J, Young L, McGuire W. Slow advancement of enteral feed volumes to prevent necrotising enterocolitis in very low birth weight infants. Cochrane Database Syst Rev 2014;12:CD001241.
39. Konnikova Y, Zaman MM, Makda M, D'Onofrio D, Freedman SD, Martin CR. Late enteral feedings are associated with intestinal inflammation and adverse neonatal outcomes. PLoS One 2015;10:e0132924.
40. Burrin DG, Stoll B, Jiang R, Chang X, Hartmann B, Holst JJ, Greeley GH Jr., Reeds PJ. Minimal enteral nutrient requirements for intestinal growth in neonatal piglets: how much is enough? Am J Clin Nutr 2000;71:1603-10.
41. Lucas A, Cole TJ. Breast milk and neonatal necrotising enterocolitis. Lancet 1990;336:1519-23.
42. Meier PP, Johnson TJ, Patel AL, Rossman B. Evidence-based methods that promote human milk feeding of preterm infants: an expert review. Clin Perinatol 2017;44:1-22.
43. Gothefors L, Blenkharn I. Clostridium butyricum and necrotizing enterocolitis. Lancet 1978;311:52-3.
44. Bouvet P, Ferraris L, Dauphin B, Popoff MR, Butel MJ, Aires J. 16S rRNA gene sequencing, multilocus sequence analysis, and mass spectrometry identification of the proposed new species "Clostridium neonatale". J Clin Microbiol 2014;52:4129-36.
45. Brower-Sinning R, Zhong D, Good M, Firek B, Baker R, Sodhi CP, Hackam DJ, Morowitz MJ. Mucosa-associated bacterial diversity in necrotizing enterocolitis. PLoS One 2014;9:e105046.
46. Waligora-Dupriet AJ, Dugay A, Auzeil N, Nicolis I, Rabot S, Huerre MR, Butel MJ. Short-chain fatty acids and polyamines in the pathogenesis of necrotizing enterocolitis: kinetics aspects in gnotobiotic quails. Anaerobe 2009;15:138-44.
47. Heida FH, Harmsen HJ, Timmer A, Kooi EM, Bos AF, Hulscher JB. Identification of bacterial invasion in necrotizing enterocolitis specimens using fluorescent in situ hybridization. J Perinatol 2017;37:67-72.
48. Ward DV, Scholz M, Zolfo M, Taft DH, Schibler KR, Tett A, Segata N, Morrow AL. Metagenomic sequencing with strain-level resolution implicates uropathogenic E. coli in necrotizing enterocolitis and mortality in preterm infants. Cell Reports 2016;14:2912-24.
49. Pammi M, Cope J, Tarr PI, Warner BB, Morrow AL, Mai V, Gregory KE, Kroll JS, McMurtry V, Ferris MJ, et al. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: a systematic review and meta-analysis. Microbiome 2017;5:31-46.
50. Stewart CJ, Nicholas D, Embleton NDL, Marrs EC, Smith DP, Nelson A, Abdulkadir B, Skeath T, Petrosino JF, Perry JD, et al. Temporal bacterial and metabolic development of the preterm gut reveals specific signatures in health and disease. Microbiome 2016;4:67-76.