Effects of probiotic supplementation on the gut microbiota and antibiotic resistome development in preterm infants

Frontiers in Pediatrics

Volumn 6, Issue , 2018, Pages

  Esaiassen, Eirin ^a,b   Hjerde, Erik ^a   Cavanagh, Jorunn Pauline ^a,b   Pedersen, Tanja ^c   Andresen, Jannicke H ^d   Rettedal, Siren I ^e   Støen, Ragnhild ^f,g   Nakstad, Britt ^h,i   Willassen, Nils P ^a   Klingenberg, Claus ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

^e STAVANGER UNIVERSITY HOSPITAL   (Norway)

^f TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

^g NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^h AKERSHUS UNIVERSITY HOSPITAL   (Norway)

ⁱ UNIVERSITY OF OSLO   (Norway)

Author keywords

Bifidobacteria; Colonization resistance; Gut microbiota; Lactobacilli; Preterm infant; Shotgun metagenome sequencing; Taxonomy

Indexed keywords

EID: 85058213664     PISSN: None     EISSN: 22962360     Source Type: Journal    
DOI: 10.3389/fped.2018.00347     Document Type: Article

References (61)

1. Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: a research priority. Microbiome (2014) 2:38. doi: 10.1186/2049-2618-2-38
2. Olin A, Henckel E, Chen Y, Lakshmikanth T, Pou C,Mikes J, et al. Stereotypic immune systemdevelopment in newborn children. Cell (2018) 5:1277-92.e14. doi: 10.1016/j.cell.2018.06.045
3. Pammi M, Cope J, Tarr PI, Warner BB, Morrow AL, Mai V, et al. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: a systematic review and meta-analysis. Microbiome (2017) 1:31. doi: 10.1186/s40168-017-0248-8
4. AlFaleh K, Anabrees J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. (2014) 10:CD005496. doi: 10.1002/14651858.CD005496. pub4
5. Aceti A, Gori D, Barone G, Callegari ML, Di Mauro A, Fantini MP, et al. Probiotics for prevention of necrotizing enterocolitis in preterm infants: systematic review and meta-analysis. Ital J Pediatr. (2015) 41:89. doi: 10.1186/s13052-015-0199-2
6. Sawh SC, Deshpande S, Jansen S, Reynaert CJ, Jones PM. Prevention of necrotizing enterocolitis with probiotics: a systematic review and metaanalysis. PeerJ. (2016) 4:e2429. doi: 10.7717/peerj.2429
7. Lau CS, Chamberlain RS. Probiotic administration can prevent necrotizing enterocolitis in preterm infants: a meta-analysis. J Pediatr Surg. (2015) 8:1405-12. doi: 10.1016/j.jpedsurg.2015.05.008
8. Olsen R, Greisen G, Schroder M, Brok J. Prophylactic probiotics for preterm infants: a systematic review and meta-analysis of observational studies. Neonatology (2016) 2:105-12. doi: 10.1159/000441274
9. Costeloe K, Bowler U, Brocklehurst P, Hardy P, Heal P, Juszczak E, et al. A randomised controlled trial of the probiotic Bifidobacterium breve BBG-001 in preterm babies to prevent sepsis, necrotising enterocolitis and death: the Probiotics in Preterm infantS (PiPS) trial. Health Technol Assess. (2016) 66:1-194. doi: 10.3310/hta20660
10. Denkel LA, Schwab F, Garten L, Geffers C, Gastmeier P, Piening B. Protective effect of dual-strain probiotics in preterm infants: a multi-center time series analysis. PLoS ONE (2016) 6:e0158136. doi: 10.1371/journal.pone.0158136
11. Tarnow-Mordi W, Soll RF. Probiotic supplementation in preterm infants: it is time to change practice. J Pediatr. (2014) 5:959-60. doi: 10.1016/j.jpeds.2013.12.050
12. Viswanathan S, Lau C, Akbari H, Hoyen C, Walsh MC. Survey and evidence based review of probiotics used in very low birth weight preterm infants within the United States. J Perinatol. (2016) 12:1106-11. doi: 10.1038/jp.2016.144
13. Esaiassen E, Cavanagh P, Hjerde E, Simonsen GS, Stoen R, Klingenberg C. Bifidobacterium longum subspecies infantis bacteremia in 3 extremely preterm infants receiving probiotics. Emerg Infect Dis. (2016) 9:1664-6. doi: 10.3201/eid2209.160033
14. Zbinden A, Zbinden R, Berger C, Arlettaz R. Case series of Bifidobacterium longumbacteremia in three preterm infants on probiotic therapy.Neonatology (2015) 1:56-9. doi: 10.1159/000367985
15. Kolacek S, Hojsak I, Berni Canani R, Guarino A, Indrio F, et al. Commercial probiotic products: a call for improved quality control. a position paper by the ESPGHAN working group for probiotics and prebiotics. J Pediatr Gastroenterol Nutr. (2017) 1:117-24. doi: 10.1097/mpg.0000000000001603
16. Vallabhaneni S, Walker TA, Lockhart SR, Ng D, Chiller T, Melchreit R, et al. Notes from the field: fatal gastrointestinal mucormycosis in a premature infant associated with a contaminated dietary supplement-Connecticut, 2014. MMWR Morb MortalWkly Rep. (2015) 6:155-6
17. Frost BL, Modi BP, Jaksic T, Caplan MS. New medical and surgical insights into neonatal necrotizing enterocolitis: a review. JAMA Pediatr. (2017) 1:83-8. doi: 10.1001/jamapediatrics.2016.2708
18. Hsieh EM, Hornik CP, Clark RH, Laughon MM, Benjamin DK Jr, Smith PB. Medication use in the neonatal intensive care unit. Am J Perinatol. (2014) 9:811-21. doi: 10.1055/s-0033-1361933
19. Esaiassen E, Fjalstad JW, Juvet LK, van den Anker JN, Klingenberg C. Antibiotic exposure in neonates and early adverse outcomes: a systematic review and meta-analysis. J Antimicrob Chemother. (2017) 72:1858-70. doi: 10.1093/jac/dkx088
20. Cotten CM, Taylor S, Stoll B, Goldberg RN, Hansen NI, Sanchez PJ, et al. Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics (2009) 1:58-66. doi: 10.1542/peds.2007-3423
21. Gibson MK, Wang B, Ahmadi S, Burnham CA, Tarr PI, Warner BB, et al. Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome. Nat Microbiol. (2016) 1:16024. doi: 10.1038/nmicrobiol.2016.24
22. Fjalstad JW, Esaiassen E, Juvet LK, van den Anker JN, Klingenberg C. Antibiotic therapy in neonates and impact on gut microbiota and antibiotic resistance development: a systematic review. J Antimicrob Chemother. (2017) 73:569-80. doi: 10.1093/jac/dkx426
23. Kelly BJ, Gross R, Bittinger K, Sherrill-Mix S, Lewis JD, Collman RG, et al. Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOV. Bioinformatics (2015) 15:2461-8. doi: 10.1093/bioinformatics/btv183
24. Klingenberg C. Preterm Infant Gut (PINGU)-a Norwegian Multi Centre Study (PINGU). Available online at: https://clinicaltrials.gov/ct2/show/ NCT02197468
25. Hill CJ, Brown JR, LynchDB, Jeffery IB, Ryan CA, Ross RP, et al. Effect of room temperature transport vials on DNA quality and phylogenetic composition of faecal microbiota of elderly adults and infants. Microbiome (2016) 1:19. doi: 10.1186/s40168-016-0164-3
26. Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. (2011) 3:255-64. doi: 10.1056/NEJMra1005408
27. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods (2015) 10:902-3. doi: 10.1038/nmeth.3589
28. McArthur AG,Waglechner N, NizamF, Yan A, AzadMA, Baylay AJ, et al. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother. (2013) 7:3348-57. doi: 10.1128/aac.00419-13
29. Kaminski J, Gibson MK, Franzosa EA, Segata N, Dantas G, Huttenhower C. High-specificity targeted functional profiling in microbial communities with shortBRED. PLoS Comput Biol. (2015) 12:e1004557. doi: 10.1371/journal.pcbi.1004557
30. Klingenberg C. Manual of Neonatal Medicine. 5th Edn. Tromsø: Paediatric Deptartment, University Hospital of Northern Norway (2017)
31. Abdulkadir B, Nelson A, Skeath T, Marrs EC, Perry JD, Cummings SP, et al. Routine use of probiotics in preterm infants: longitudinal impact on the microbiome and metabolome. Neonatology (2016) 4:239-47. doi: 10.1159/000442936
32. de Man P, Verhoeven BA, Verbrugh HA, Vos MC, van den Anker JN. An antibiotic policy to prevent emergence of resistant bacilli. Lancet (2000) 9208:973-8. doi: 10.1016/S0140-6736(00)90015-1
33. Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics (2014) 21:3123-4. doi: 10.1093/bioinformatics/btu494
34. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B (1995) 57:289-300
35. Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res. (2007) 3:377-86. doi: 10.1101/gr.5969107
36. Weng M, Walker WA. The role of gut microbiota in programming the immune phenotype. J Dev Orig Health Dis. (2013) 3:203-14. doi: 10.1017/s2040174412000712
37. Hill CJ, Lynch DB, Murphy K, Ulaszewska M, Jeffery IB, O'Shea CA, et al. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome (2017) 1:4. doi: 10.1186/s40168-016-0213-y
38. Arboleya S, Binetti A, Salazar N, Fernandez N, Solis G, Hernandez-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol. (2012) 3:763-72. doi: 10.1111/j.1574-6941.2011.01261.x
39. Stewart CJ, Embleton ND, Marrs EC, Smith DP, Nelson A, Abdulkadir B, et al. Temporal bacterial and metabolic development of the preterm gut reveals specific signatures in health and disease. Microbiome (2016) 1:67. doi: 10.1186/s40168-016-0216-8
40. Jacobs SE, Tobin JM, Opie GF, Donath S, Tabrizi SN, PirottaM, et al. Probiotic effects on late-onset sepsis in very preterm infants: a randomized controlled trial. Pediatrics (2013) 6:1055-62. doi: 10.1542/peds.2013-1339
41. Bertelli C, Pillonel T, Torregrossa A, Prod'hom G, Fischer CJ, Greub G, et al. Bifidobacterium longum bacteremia in preterm infants receiving probiotics. Clin Infect Dis. (2015) 6:924-7. doi: 10.1093/cid/ciu946
42. 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) 8:944-54. doi: 10.1038/ismej. 2009.37
43. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, et al. Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. J Pediatr Gastroenterol Nutr. (2007) 5:577-82. doi: 10.1097/MPG.0b013e3180406b20
44. Swidsinski A, Loening-Baucke V, Lochs H, Hale LP. Spatial organization of bacterial flora in normal and inflamed intestine: a fluorescence in situ hybridization study in mice. World J Gastroenterol. (2005) 8:1131-40. doi: 10.3748/wjg.v11.i8.1131
45. Villmones HC, Haug ES, Ulvestad E, Grude N, Stenstad T, Halland A, et al. Species level description of the human ileal bacterial microbiota. Sci Rep. (2018) 1:4736. doi: 10.1038/s41598-018-23198-5
46. Dutta S, Ray P, Narang A. Comparison of stool colonization in premature infants by three dose regimes of a probiotic combination: a randomized controlled trial. Am J Perinatol. (2015) 8:733-40. doi: 10.1055/s-0034-1395473
47. 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) 10019:649-60. doi: 10.1016/s0140-6736(15)01027-2
48. Gritz EC, Bhandari V. The human neonatal gut microbiome: a brief review. Front Pediatr. (2015) 3:17. doi: 10.3389/fped.2015.00017
49. Deshpande GC, Rao SC, Keil AD, Patole SK. Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med. (2011) 9:92. doi: 10.1186/1741-7015-9-92
50. Siggers RH, Siggers J, Thymann T, Boye M, Sangild PT. Nutritional modulation of the gut microbiota and immune system in preterm neonates susceptible to necrotizing enterocolitis. J Nutr Biochem. (2011) 6:511-21. doi: 10.1016/j.jnutbio.2010.08.002
51. Cilieborg MS, Boye M, Sangild PT. Bacterial colonization and gut development in preterm neonates. Early Hum Dev. (2012) 88:S41-9. doi: 10.1016/j.earlhumdev.2011.12.027
52. Watkins C, Murphy K, Dempsey EM, O'Shea CA, Murphy BP, O'Toole PW, et al. Dose-interval study of a dual probiotic in preterm infants. Arch Dis Child Fetal Neonatal Ed. (2018) 20:313468. doi: 10.1136/archdischild-2017-313468
53. Hall MA, Cole CB, Smith SL, Fuller, Rolles CJ. Factors influencing the presence of faecal lactobacilli in early infancy. Arch Dis Childhood (1990) 2:185-88
54. Fouhy F, Guinane CM, Hussey S, Wall R, Ryan CA, Dempsey EM, et al. High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother. (2012) 11:5811-20. doi: 10.1128/aac.00789-12
55. Rose G, Shaw AG, Sim K, Wooldridge DJ, Li MS, Gharbia S, et al. Antibiotic resistance potential of the healthy preterm infant gut microbiome. PeerJ. (2017) 5:e2928. doi: 10.7717/peerj.2928
56. Grazul H, Kanda LL, Gondek D. Impact of probiotic supplements on microbiome diversity following antibiotic treatment of mice. Gut Microbes (2016) 2:101-14. doi: 10.1080/19490976.2016.1138197
57. Fouhy F, Ogilvie LA, Jones B, Ross RP, Ryan AC, Dempsey EM, et al. Identification of aminoglycoside and beta-lactamresistance genes fromwithin an infant gut functional metagenomic library. PLoS ONE (2014) 9:e108016. doi: 10.1371/journal.pone.0108016
58. von Wintersdorff CJ, Wolffs PF, Savelkoul PH, Nijsen RR, Lau S, Gerhold K, et al. The gut resistome is highly dynamic during the first months of life. Future Microbiol. (2016) 4:501-10. doi: 10.2217/fmb.15.154
59. Moore AM, Patel S, Forsberg KJ, Wang B, Bentley G, Razia Y, et al. Pediatric fecal microbiota harbor diverse and novel antibiotic resistance genes. PLoS ONE (2013) 11:e78822. doi: 10.1371/journal.pone.0078822
60. Pamer EG. Resurrecting the intestinal microbiota to combat antibioticresistant pathogens. Science (2016) 6285:535-8. doi: 10.1126/science.aad9382
61. Ravi A, Estensmo ELF, Abee-Lund TML, Foley SL, Allgaier B, Martin CR, et al. Association of the gut microbiota mobilome with hospital location and birth weight in preterm infants. Pediatr Res. (2017) 82:829-838. doi: 10.1038/pr.2017.146