Clostridial strain-specific characteristics associated with necrotizing enterocolitis

Applied and Environmental Microbiology

Volumn 84, Issue 7, 2018, Pages

  Schönherr Hellec, Sophia ^a   Klein, Geraldine L ^a   Delannoy, Johanne ^a   Ferraris, Laurent ^a   Rozé, Jean Christophe ^b   Butel, Marie José ^a   Aires, Julio ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Clostridia; Clostridium butyricum; Clostridium neonatale; Necrotizing enterocolitis; Preterm neonates

Indexed keywords

BACTERIA; CYTOTOXICITY; DISCRIMINANT ANALYSIS;

CELLULAR CYTOTOXICITY; CLOSTRIDIUM BUTYRICUM; EXPLANATORY VARIABLES; GASTROINTESTINAL TRACT; NECROTIZING ENTEROCOLITIS; PRETERM NEONATES; STRAIN CHARACTERISTICS; STRAIN SIGNATURES;

CLOSTRIDIUM;

BACTERIUM; CELL; DISCRIMINANT ANALYSIS; FECES; GASTROENTERITIS; PHENOTYPE; SEPARATION; SURVIVAL; TOXICITY;

BACTERIA (MICROORGANISMS); CLOSTRIDIA; CLOSTRIDIUM BUTYRICUM; CLOSTRIDIUM NEONATALE;

CACO-2 CELL LINE; CLINICAL TRIAL; CLOSTRIDIUM; CLOSTRIDIUM INFECTION; COHORT ANALYSIS; FECES; FRANCE; HUMAN; MICROBIOLOGY; MULTICENTER STUDY; NECROTIZING ENTEROCOLITIS; NEWBORN; PHYSIOLOGY;

CACO-2 CELLS; CLOSTRIDIUM; CLOSTRIDIUM INFECTIONS; COHORT STUDIES; ENTEROCOLITIS, NECROTIZING; FECES; FRANCE; HUMANS; INFANT, NEWBORN;

EID: 85044121501     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02428-17     Document Type: Article

References (30)

1. Blencowe H, Cousens S, Chou D, Oestergaard MZ, Say L, Moller AB, Kinney M, Lawn J. 2012. 15 million preterm births: priorities for action based on national, regional and global estimates, p 17-31. In Howson CP, Kinney MV, Lawn JE (ed), Born too soon: the global action report on preterm birth. World Health Organization, Geneva, Switzerland
2. Niño DF, Sodhi CP, Hackam DJ. 2016. Necrotizing enterocolitis: new insights into pathogenesis and mechanisms. Nat Rev Gastroenterol Hepatol 13:590-600. https://doi.org/10.1038/nrgastro.2016.119
3. Pammi M, Cope J, Tarr PI, Warner BB, Morrow AL, Mai V, Gregory KE, Kroll JS, McMurtry V, Ferris MJ, Engstrand L, Lilja HE, Hollister EB, Versalovic J, Neu J. 2017. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: a systematic review and meta-analysis. Microbiome 5:31. https://doi.org/10.1186/s40168-017-0248-8
4. Cho SX, Berger PJ, Nold-Petry CA, Nold MF. 2016. The immunological landscape in necrotising enterocolitis. Expert Rev Mol Med 18:e12. https://doi.org/10.1017/erm.2016.13
5. Rozé J-C, Ancel P-Y, Lepage P, Martin-Marchand L, Nabhani ZA, Delannoy J, Picaud J-C, Lapillonne A, Aires J, Durox M, Darmaun D, Neu J, Butel M-J, Nutrition EPIPAGE 2 Study Group, EPIFLORE Study Group. 2017. Nutritional strategies and gut microbiota composition as risk factors for necrotizing enterocolitis in very-preterm infants. Am J Clin Nutr 106: 821-830. https://doi.org/10.3945/ajcn.117.152967
6. Alexander VN, Northrup V, Bizzarro MJ. 2011. Antibiotic exposure in the newborn intensive care unit and the risk of necrotizing enterocolitis. J Pediatr 159:392-397. https://doi.org/10.1016/j.jpeds.2011.02.035
7. Sangild PT, Siggers RH, Schmidt M, Elnif J, Bjornvad CR, Thymann T, Grondahl ML, Hansen AK, Jensen SK, Boye M, Moelbak L, Buddington RK, Weström BR, Holst JJ, Burrin DG. 2006. Diet-and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130:1776-1792. https://doi.org/10.1053/j .gastro.2006.02.026
8. Cassir N, Benamar S, Khalil JB, Croce O, Saint-Faust M, Jacquot A, Million M, Azza S, Armstrong N, Henry M, Jardot P, Robert C, Gire C, Lagier J-C, Chabrière E, Ghigo E, Marchandin H, Sartor C, Boutte P, Cambonie G, Simeoni U, Raoult D, Scola BL. 2015. Clostridium butyricum strains and dysbiosis linked to necrotizing enterocolitis in preterm neonates. Clin Infect Dis 61:1107-1115. https://doi.org/10.1093/cid/civ468
9. Coggins SA, Wynn JL, Weitkamp J-H. 2015. Infectious causes of necrotizing enterocolitis. Clin Perinatol 42:133-154. https://doi.org/10.1016/j .clp.2014.10.012
10. Ferraris L, Butel MJ, Campeotto F, Vodovar M, Rozé JC, Aires J. 2012. Clostridia in premature neonates' gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization. PLoS One 7:e30594. https://doi.org/10.1371/journal.pone.0030594
11. Alfa MJ, Robson D, Davi M, Bernard K, Van Caeseele P, Harding GKM. 2002. An outbreak of necrotizing enterocolitis associated with a novel Clostridium species in a neonatal intensive care unit. Clin Infect Dis 35:S101-S105. https://doi.org/10.1086/341929
12. Han VKM, Sayed H, Chance GW, Brabyn DG, Shaheed WA. 1983. An outbreak of Clostridium difficile necrotizing enterocolitis: a case for oral vancomycin therapy?. Pediatrics 71:935-941
13. Heida FH, van Zoonen AGJF, Hulscher JBF, te Kiefte BJC, Wessels R, Kooi EMW, Bos AF, Harmsen HJM, de Goffau MC. 2016. A necrotizing enterocolitis-associated gut microbiota is already present in the meconium: results of a prospective study. Clin Infect Dis 62:863-870. https://doi.org/10.1093/cid/ciw016
14. Sim K, Shaw AG, Randell P, Cox MJ, McClure ZE, Li M-S, Haddad M, Langford PR, Cookson WOCM, Moffatt MF, Kroll JS. 2015. Dysbiosis anticipating necrotizing enterocolitis in very premature infants. Clin Infect Dis 60:389-397. https://doi.org/10.1093/cid/ciu822
15. Zhou Y, Shan G, Sodergren E, Weinstock G, Walker WA, Gregory KE. 2015. Longitudinal analysis of the premature infant intestinal microbiome prior to necrotizing enterocolitis: a case-control study. PLoS One 10: e0118632. https://doi.org/10.1371/journal.pone.0118632
16. Dittmar E, Beyer P, Fischer D, Schäfer V, Schoepe H, Bauer K, Schlösser R. 2008. Necrotizing enterocolitis of the neonate with Clostridium perfringens: diagnosis, clinical course, and role of alpha toxin. Eur J Pediatr 167:891-895. https://doi.org/10.1007/s00431-007-0614-9
17. Smith B, Bodé S, Petersen BL, Jensen TK, Pipper C, Kloppenborg J, Boyé M, Krogfelt KA, Mølbak L. 2011. Community analysis of bacteria colonizing intestinal tissue of neonates with necrotizing enterocolitis. BMC Microbiol 11:73. https://doi.org/10.1186/1471-2180-11-73
18. de la Cochetière M-F, Piloquet H, des Robert C, Darmaun D, Galmiche J-P, Rozé J-C. 2004. Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 56:366-370. https://doi.org/10.1203/01.PDR.0000134251.45878.D5
19. Tomas CA, Welker NE, Papoutsakis ET. 2003. Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell's transcriptional program. Appl Environ Microbiol 69:4951-4965. https://doi.org/ 10.1128/AEM.69.8.4951-4965.2003
20. Zhang L, Nie X, Ravcheev DA, Rodionov DA, Sheng J, Gu Y, Yang S, Jiang W, Yang C. 2014. Redox-responsive repressor Rex modulates alcohol production and oxidative stress tolerance in Clostridium acetobutylicum. J Bacteriol 196:3949-3963. https://doi.org/10.1128/JB.02037-14
21. Kawasaki S, Nakagawa T, Nishiyama Y, Benno Y, Uchimura T, Komagata K, Kozaki M, Niimura Y. 1998. Effect of oxygen on the growth of Clostridium butyricum (type species of the genus Clostridium), and the distribution of enzymes for oxygen and for active oxygen species in clostridia. J Ferment Bioeng 86:368-372. https://doi.org/10.1016/S0922-338X(99)89006-0
22. Imlay JA. 2002. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 46:111-153. https://doi.org/ 10.1016/S0065-2911(02)46003-1
23. Neuhaus FC, Baddiley J. 2003. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686-723. https://doi.org/10.1128/MMBR.67.4.686-723.2003
24. Mogensen TH. 2009. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240-273. https://doi .org/10.1128/CMR.00046-08
25. Sturm R, Staneck JL, Stauffer LR, Neblett WW. 1980. Neonatal necrotizing enterocolitis associated with penicillin-resistant, toxigenic Clostridium butyricum. Pediatrics 66:928-931
26. Popoff MR, Jolivet-Reynaud C, Carlier JP. 1987. Cytotoxic activity of Clostridium butyricum supernatants induced by butyrate. FEMS Microbiol Lett 43:95-100. https://doi.org/10.1111/j.1574-6968.1987.tb02104.x
27. Waligora-Dupriet A-J, Dugay A, Auzeil N, Huerre M, Butel M-J. 2005. Evidence for clostridial implication in necrotizing enterocolitis through bacterial fermentation in a gnotobiotic quail model. Pediatr Res 58: 629-635. https://doi.org/10.1203/01.PDR.0000180538.13142.84
28. Schönherr-Hellec S, Klein G, Delannoy J, Ferraris L, Friedel I, Rozé JC, Butel MJ, Aires J. 2017. Comparative phenotypic analysis of "Clostridium neonatale" and Clostridium butyricum isolates from neonates. Anaerobe 48:76-82. https://doi.org/10.1016/j.anaerobe.2017.07.002
29. Walsh MC, Kliegman RM. 1986. Necrotizing enterocolitis: treatment based on staging criteria. Pediatr Clin North Am 33:179-201. https://doi .org/10.1016/S0031-3955(16)34975-6
30. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an opensource platform for biological-image analysis. Nat Methods 9:676-682. https://doi.org/10.1038/nmeth.2019