Probiotics for prevention of necrotizing enterocolitis in preterm infants: systematic review and meta-analysis

Italian Journal of Pediatrics

Volumn 41, Issue 1, 2015, Pages

  Aceti, Arianna ^a   Gori, Davide ^b   Barone, Giovanni ^c   Callegari, Maria Luisa ^d   Di Mauro, Antonio ^e   Fantini, Maria Pia ^b   Indrio, Flavia ^e   Maggio, Luca ^c   Meneghin, Fabio ^f   Morelli, Lorenzo ^d   Zuccotti, Gianvincenzo ^f   Corvaglia, Luigi ^a   Italian Society of Neonatology, ^g  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

^e UNIVERSITY OF BARI   (Italy)

^f UNIVERSITY OF MILAN   (Italy)

^g NONE

Author keywords

Meta analysis; Necrotizing enterocolitis; Newborn; Probiotics

Indexed keywords

PROBIOTIC AGENT;

ARTICLE; BACILLUS COAGULANS; BACTERIAL STRAIN; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; CLINICAL EVALUATION; DISEASE SEVERITY; DRUG EFFECT; HIGH RISK POPULATION; HUMAN; LACTOBACILLUS; LACTOBACILLUS REUTERI; LACTOBACILLUS SPOROGENES; META ANALYSIS; NECROTIZING ENTEROCOLITIS; NONHUMAN; PREMATURITY; SACCHAROMYCES BOULARDII; SYSTEMATIC REVIEW; TREATMENT OUTCOME; VERY LOW BIRTH WEIGHT; ENTEROCOLITIS, NECROTIZING; INFANT, PREMATURE, DISEASES; NEWBORN;

ENTEROCOLITIS, NECROTIZING; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INFANT, PREMATURE, DISEASES; PROBIOTICS; TREATMENT OUTCOME;

EID: 84946834291     PISSN: 17208424     EISSN: 18247288     Source Type: Journal    
DOI: 10.1186/s13052-015-0199-2     Document Type: Article

References (67)

1. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011;364:255-64.
2. Bisquera JA, Cooper TR, Berseth CL. Impact of necrotizing enterocolitis on length of stay and hospital charges in very low birth weight infants. Pediatrics. 2002;109:423-8.
3. Gephart S, McGrath J, Effken J, Halpern M. Necrotizing enterocolitis risk: state of the science. Adv Neonatal Care. 2012;12:77-89.
4. Sanders ME, Guarner F, Guerrant R, Holt PR, Quigley EMM, Sartor RB, et al. An update on the use and investigation of probiotics in health and disease. Gut. 2013;62:787-96.
5. Martin CR, Walker WA. Probiotics: role in pathophysiology and prevention in necrotizing enterocolitis. Semin Perinatol. 2008;32:127-37.
6. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3:e3056.
7. 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;156:20-5.
8. Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, et al. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J. 2009;3:944-54.
9. Murguía-Peniche T, Mihatsch WA, Zegarra J, Supapannachart S, Ding Z-Y, Neu J. Intestinal mucosal defense system, Part 2. Probiotics and prebiotics. J Pediatr. 2013;162(3 Suppl):S64-71.
10. Deshpande G, Rao S, Patole S, Bulsara M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics. 2010;125:921-30.
11. Alfaleh K, Anabrees J, Bassler D. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2014;4:CD005496. doi: 10.1002/14651858.CD005496.pub4.
12. Thomas DW, Greer FR. Probiotics and prebiotics in pediatrics. Pediatrics. 2010;126:1217-31.
13. Mihatsch WA, Braegger CP, Decsi T, Kolacek S, Lanzinger H, Mayer B, et al. Critical systematic review of the level of evidence for routine use of probiotics for reduction of mortality and prevention of necrotizing enterocolitis and sepsis in preterm infants. Clin Nutr. 2012;31:6-15.
14. Szajewska H. Probiotics and prebiotics in preterm infants: where are we? Where are we going? Early Hum Dev. 2010;86 Suppl 1:81-6.
15. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506-14.
16. FAO, WHO. Probiotics in food. Health and nutritional properties and guidelines for evaluation. 2006.
17. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.
18. Bell MJ, Ternberg JL, Feigin RD, Keating JP, Marshall R, Barton L, et al. Neonatal necrotizing enterocolitis: therapeutic decisions based upon clinical staging. Ann Surg. 1978;187:1-7.
19. Walsh MC, Kliegman RM. Necrotizing enterocolitis: treatment based on staging criteria. Pediatr Clin North Am. 1986;33:179-201.
20. Greenhalgh T, Peacock R. Effectiveness and efficiency of search methods in systematic reviews of complex evidence: audit of primary sources. BMJ. 2005;331:1064-5.
21. Cochrane handbook for systematic reviews of interventions. [ http://handbook.cochrane.org/ ].
22. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924-6.
23. Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions. Version 5.1.0 (March 2011). 2011.
24. Hardy RJ, Thompson SG. Detecting and describing heterogeneity in meta-analysis. Stat Med. 1998;17:841-56.
25. Oncel MY, Sari FN, Arayici S, Guzoglu N, Erdeve O, Uras N, et al. Lactobacillus Reuteri for the prevention of necrotising enterocolitis in very low birthweight infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2014;99:F110-5.
26. Jacobs SE, Tobin JM, Opie GF, Donath S, Tabrizi SN, Pirotta M, et al. Probiotic effects on late-onset sepsis in very preterm infants: a randomized controlled trial. Pediatrics. 2013;132:1055-62.
27. Serce O, Benzer D, Gursoy T, Karatekin G, Ovali F. Efficacy of saccharomyces boulardii on necrotizing enterocolitis or sepsis in very low birth weight infants: a randomised controlled trial. Early Hum Dev. 2013;89:1033-6.
28. Demirel G, Erdeve O, Celik IH, Dilmen U. Saccharomyces boulardii for prevention of necrotizing enterocolitis in preterm infants: a randomized, controlled study. Acta Paediatr. 2013;102:560-5.
29. Benor S, Marom R, Ben Tov A, Domany KA, Zaidenberg-Israeli G, Dollberg S. Probiotic supplementation in mothers of very low birth weight infants. Am J Perinatol. 2014;31:497-504.
30. Rojas MA, Lozano JM, Rojas MX, Rodriguez VA, Rondon MA, Bastidas JA, et al. Prophylactic probiotics to prevent death and nosocomial infection in preterm infants. Pediatrics. 2012;130:e1113-20.
31. Sari FN, Eras Z, Dizdar EA, Erdeve O, Oguz SS, Uras N, et al. Do oral probiotics affect growth and neurodevelopmental outcomes in very low-birth-weight preterm infants? Am J Perinatol. 2012;29:579-86.
32. Fernández-Carrocera LA, Solis-Herrera A, Cabanillas-Ayón M, Gallardo-Sarmiento RB, García-Pérez CS, Montaño-Rodríguez R, et al. Double-blind, randomised clinical assay to evaluate the efficacy of probiotics in preterm newborns weighing less than 1500 g in the prevention of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed. 2013;98:F5-9.
33. Al-Hosni M, Duenas M, Hawk M, Stewart LA, Borghese RA, Cahoon M, et al. Probiotics-supplemented feeding in extremely low-birth-weight infants. J Perinatol. 2012;32:253-9.
34. Sari FN, Dizdar EA, Oguz S, Erdeve O, Uras N, Dilmen U. Oral probiotics: Lactobacillus sporogenes for prevention of necrotizing enterocolitis in very low-birth weight infants: a randomized, controlled trial. Eur J Clin Nutr. 2011;65:434-9.
35. Braga TD, da Silva GAP, de Lira PI, de Carvalho LM. Efficacy of Bifidobacterium breve and Lactobacillus casei oral supplementation on necrotizing enterocolitis in very-low-birth-weight preterm infants: a double-blind, randomized, controlled trial. Am J Clin Nutr. 2011;93:81-6.
36. Awad H, Mokhtar H, Imam SS, Gad GI, Hafez H, Aboushady N. Comparison between killed and living probiotic usage versus placebo for the prevention of necrotizing enterocolitis and sepsis in neonates. Pak J Biol Sci. 2010;13:253-62.
37. Lin H-C, Hsu C-H, Chen H-L, Chung M-Y, Hsu J-F, Lien R, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics. 2008;122:693-700.
38. Samanta M, Sarkar M, Ghosh P, Ghosh JK, Sinha MK, Chatterjee S. Prophylactic probiotics for prevention of necrotizing enetrocolitis in very low birth weight newborns. J Trop Pediatr. 2008;55:128-31.
39. Stratiki Z, Costalos C, Sevastiadou S, Kastanidou O, Skouroliakou M, Giakoumatou A, et al. The effect of a bifidobacter supplemented bovine milk on intestinal permeability of preterm infants. Early Hum Dev. 2007;83:575-9.
40. Bin-Nun A, Bromiker R, Wilschanski M, Kaplan M, Rudensky B, Caplan M, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates. J Pediatr. 2005;147:192-6.
41. Lin H-C, Su B-H, Chen A-C, Lin T-W, Tsai C-H, Yeh T-F, et al. Oral probiotics reduce the incidence and severity of necrotizing enterocolitis in very low birth weight infants. Pediatrics. 2005;115:1-4.
42. Dani C, Biadaioli R, Bertini G, Martelli E, Rubaltelli FF. Probiotics feeding in prevention of urinary tract infection, bacterial sepsis and necrotizing enterocolitis in preterm infants. Biol Neonate. 2002;82:103-8.
43. Mihatsch WA, Vossbeck S, Eikmanns B, Hoegel J, Pohlandt F. Effect of Bifidobacterium lactis on the incidence of nosocomial infections in very-low-birth-weight infants: a randomized controlled trial. Neonatology. 2010;98:156-63.
44. Dilli D, Aydin B, Fettah N, Özyazici E, Beken S, Zenciroʇlu A, et al. The ProPre-Save study: effects of probiotics and prebiotics alone or combined on necrotizing enterocolitis in very low birth weight infants €. J Pediatr. 2015. In press.
45. Patole S, Keil AD, Chang A, Nathan E, Doherty D, Simmer K, et al. Effect of Bifidobacterium breve M-16 V supplementation on fecal bifidobacteria in preterm neonates - a randomised double blind placebo controlled trial. PLoS One. 2014;9:e89511.
46. Totsu S, Yamasaki C, Terahara M, Uchiyama A, Kusuda S. Bifidobacterium and enteral feeding in preterm infants: Cluster-randomized trial. Pediatr Int. 2014;56:714-9.
47. Sehgal A, Mak W, Dunn M, Kelly E, Whyte H, McCrindle B, et al. Haemodynamic changes after delivery room surfactant administration to very low birth weight infants. Arch Dis Child Fetal Neonatal Ed. 2010;95:F345-51.
48. Saengtawesin V, Tangpolkaiwalsak R, Kanjanapattankul W. Effect of oral probiotics supplementation in the prevention of necrotizing enterocolitis among very low birth weight preterm infants. J Med Assoc Thai. 2014;97:S20-5.
49. Costalos C, Skouteri V, Gounaris A, Sevastiadou S, Triandafilidou A, Ekonomidou C, et al. Enteral feeding of premature infants with Saccharomyces boulardii. Early Hum Dev. 2003;74:89-96.
50. Rougé C, Piloquet H, Butel M-J, Berger B, Rochat F, Ferraris L, et al. Oral supplementation with probiotics in very-low-birth-weight preterm infants: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr. 2009;89:1828-35.
51. Manzoni P, Mostert M, Leonessa ML, Priolo C, Farina D, Monetti C, et al. Oral supplementation with Lactobacillus casei subspecies rhamnosus prevents enteric colonization by Candida species in preterm neonates: a randomized study. Clin Infect Dis. 2006;42:1735-42.
52. Kitajima H, Sumida Y, Tanaka R, Yuki N, Takayama H, Fujimura M. Early administration of Bifidobacterium breve to preterm infants: randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 1997;76:F101-7.
53. Mohan R, Koebnick C, Schildt J, Schmidt S, Mueller M, Possner M, et al. Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: a double-blind, placebo-controlled, randomized study. J Clin Microbiol. 2006;44:4025-31.
54. Li Y, Shimizu T, Hosaka A, Kaneko N, Ohtsuka Y, Yamashiro Y. Effects of bifidobacterium breve supplementation on intestinal flora of low birth weight infants. Pediatr Int. 2004;46:509-15.
55. Millar MR, Bacon C, Smith SL, Walker V, Hall MA. Enteral feeding of premature infants with Lactobacillus GG. Arch Dis Child. 1993;69:483-7.
56. Reuman PD, Duckworth DH, Smith KL, Kagan R, Bucciarelli RL, Ayoub EM. Lack of effect of Lactobacillus on gastrointestinal bacterial colonization in premature infants. Pediatr Infect Dis. 1986;5:663-8.
57. Manzoni P, Rinaldi M, Cattani S, Pugni L, Romeo MG, Messner H. Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates. JAMA. 2009;302:1421-8.
58. Roy A, Chaudhuri J, Sarkar D, Ghosh P, Chakraborty S. Role of enteric supplementation of Probiotics on late-onset sepsis by Candida species in preterm low birth weight neonates: a randomized, double blind, placebo-controlled trial. N Am J Med Sci. 2014;6:50-7.
59. Alfaleh K, Anabrees J, Bassler D. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2011;3:CD005496. doi: 10.1002/14651858.CD005496.pub3.
60. Drago L, De Vecchi E. Should Lactobacillus sporogenes and Bacillus coagulans have a future? J Chemother. 2009;21:371-7.
61. Guarner F, Malagelada J-R. Gut flora in health and disease. Lancet. 2003;361:512-9.
62. Luedtke SA, Yang JT, Wild HE. Probiotics and necrotizing enterocolitis: finding the missing pieces of the probiotic puzzle. J Pediatr Pharmacol Ther. 2012;17:308-28.
63. Berrington JE, Stewart CJ, Embleton ND, Cummings SP. Gut microbiota in preterm infants: assessment and relevance to health and disease. Arch Dis Child Fetal Neonatal Ed. 2013;98:F286-90.
64. Boyd CA, Quigley MA, Brocklehurst P. Donor breast milk versus infant formula for preterm infants: systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed. 2007;92:F169-75.
65. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511-21.
66. Beattie LM, Hansen R, Barclay AR. Probiotics for preterm infants: confounding features warrant caution. Pediatrics. 2010;126:e742-3. author reply e743-5.
67. Kelsen JR, Wu GD. The gut microbiota, environment and diseases of modern society. Gut Microbes. 2012;3:374-82.