Effect of saccharomyces boulardii and mode of delivery on the early development of the gut microbial community in preterm infants

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Zeber Lubecka, Natalia ^a   Kulecka, Maria ^a   Ambrozkiewicz, Filip ^a   Paziewska, Agnieszka ^a   Lechowicz, Milosz ^b   Konopka, Ewa ^c   Majewska, Urszula ^b   Borszewska Kornacka, Maria ^b   Mikula, Michal ^d   Cukrowska, Bozena ^c   Ostrowski, Jerzy ^a,d  

^a MEDICAL CENTER FOR POSTGRADUATE EDUCATION   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c CHILDREN'S MEMORIAL HEALTH INSTITUTE   (Poland)

^d INSTITUTE OF ONCOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

PROBIOTIC AGENT; RNA 16S; BACTERIAL DNA; BACTERIAL RNA; DIAGNOSTIC KIT; RIBOSOME DNA;

ACTINOBACTERIA; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM DETECTION; BACTEROIDETES; CESAREAN SECTION; DRUG EFFICACY; DRUG RESPONSE; ENTEROCOCCUS; ESCHERICHIA COLI; FEMALE; FIRMICUTES; GENE SEQUENCE; GESTATIONAL AGE; HUMAN; INFANT; INTESTINE FLORA; MAJOR CLINICAL STUDY; MALE; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PHYLUM; PREMATURITY; PROTEOBACTERIA; PSEUDOMONAS; SACCHAROMYCES BOULARDII; STAPHYLOCOCCUS; VAGINAL DELIVERY; BACTERIUM; COMPARATIVE STUDY; CONTROLLED STUDY; DIAGNOSTIC KIT; DOUBLE BLIND PROCEDURE; FECES; GENETICS; ISOLATION AND PURIFICATION; METAGENOME; MICROBIOLOGY; NEWBORN; OBSTETRIC DELIVERY; ORAL DRUG ADMINISTRATION; RANDOMIZED CONTROLLED TRIAL; RIBOTYPING; SACCHAROMYCES; SYMBIOSIS; VALIDATION STUDY;

ADMINISTRATION, ORAL; BACTERIA; DELIVERY, OBSTETRIC; DNA, BACTERIAL; DNA, RIBOSOMAL; DOUBLE-BLIND METHOD; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; MALE; METAGENOME; PROBIOTICS; REAGENT KITS, DIAGNOSTIC; RIBOTYPING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SACCHAROMYCES; SYMBIOSIS;

EID: 84960431202     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0150306     Document Type: Article

References (65)

1. Walker WA. Initial intestinal colonization in the human infant and immune homeostasis. Ann Nutr Metab. 2013; 63 Suppl 2: 8-15. doi: 10.1159/000354907 PMID: 24217032
2. Blaut M, Clavel T. Metabolic diversity of the intestinal microbiota: implications for health and disease. J Nutr. 2007; 137: 751S-5S. PMID: 17311972
3. DiGiulio DB, Romero R, Amogan H.P., 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. doi: 10.1371/journal.pone.0003056 PMID: 18725970
4. DiGiulio DB. Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med. 2012; 17: 2-11. doi: 10.1016/j.siny.2011.10.001 PMID: 22137615
5. Aagaard K, Ma J, Antony K.M., Ganu R., Petrosino J, Versalovic J. The Placenta Harbors a Unique Microbiome. Sci Transl Med. 2014; 6: 237ra65-237ra65. doi: 10.1126/scitranslmed.3008599 PMID: 24848255
6. Arrieta M-C, Stiemsma L.T., Amenyogbe N., Brown EM, Finlay B. The intestinal microbiome in early life: health and disease. Front Immunol. 2014; 5: 427. doi: 10.3389/fimmu.2014.00427 PMID: 25250028
7. Moles L, Gómez M, Heilig H., Bustos G, Fuentes S, de Vos W, et al. Bacterial diversity in meconium of preterm neonates and evolution of their fecal microbiota during the first month of life. PLoSONE. 2013; 8: e66986. doi: 10.1371/journal.pone.0066986 PMID: 23840569
8. Claud EC, Keegan KP, Brulc J.M., Lu L., Bartels D, Glass E, et al Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Microbiome. 2013; 1: 20. doi: 10.1186/2049-2618-1-20 PMID: 24450928
9. 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; 56: 5811-5820. doi: 10. 1128/AAC.00789-12 PMID: 22948872
10. Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol. 2012; 12: 9-23. doi: 10.1038/nri3112
11. Berrington JE, Stewart CJ, Embleton N.D., Cummings SP. Gut microbiota in preterm infants: assessment and relevance to health and disease. Arch Dis Child Fetal Neonatal Ed. 2013; 98: F286-290. doi: 10.1136/archdischild-2012-302134 PMID: 23009761
12. Kostic AD, Gevers D, Siljander H., Vatanen T, Hyötyläinen T, Hämäläinen A-M, et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe. 2015; 17: 260-273. doi: 10.1016/j.chom.2015.01.001 PMID: 25662751
13. Fischer A, Whiteson K, Lazarevic V., Hibbs J, Francois P, Schrenzel J. Infant gut microbial colonization and health: recent findings from metagenomics studies. Journal of Integrated OMICS. 2012; 2. doi: 10. 5584/jiomics.v2i1.76
14. Turroni F, Peano C, Pass D.A., Foroni E., Severgnini M, Claesson MJ, et al Diversity of bifidobacteria within the infant gut microbiota. PLoSONE. 2012; 7: e36957. doi: 10.1371/journal.pone.0036957 PMID: 22606315
15. Palmer C, Bik EM, DiGiulio D.B., Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoSBiol. 2007; 5: e177. doi: 10.1371/journal.pbio.0050177 PMID: 17594176
16. Roger LC, Costabile A, Holland D.T., Hoyles L., McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology (Reading, Engl). 2010; 156: 3329-3341. doi: 10.1099/mic.0.043224-0
17. Werner JJ, Koren O, Hugenholtz P., DeSantis TZ, Walters WA, Caporaso JG, et al Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J. 2012; 6: 94-103. doi: 10.1038/ismej.2011.82 PMID: 21716311
18. Koenig JE, Spor A, Scalfone N., Fricker A D, Stombaugh J, Knight R., et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA. 2011; 108 Suppl 1: 4578-4585. doi: 10.1073/pnas.1000081107 PMID: 20668239
19. Voreades N, Kozil A, Weir TL Diet and the development of the human intestinal microbiome. Front Microbiol. 2014; 5: 494. doi: 10.3389/fmicb.2014.00494 PMID: 25295033
20. Kuitunen M, Kukkonen K, Juntunen-Backman K, Korpela R., Poussa T, Tuure T, et al Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J Allergy Clin Immunol. 2009; 123: 335-341. doi: 10.1016/j.jaci.2008.11.019 PMID: 19135235
21. Kalliomäki M., Salminen S, Poussa T., Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-yearfollow-up of a randomised placebo-controlled trial. Lancet. 2003; 361:1869-1871. doi: 10.1016/S0140-6736(03)13490-3 PMID: 12788576
22. 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. PMID: 14580749
23. Arvola T, Laiho K, Torkkeli S., Mykkänen H, Salminen S., Maunula L, et al. Prophylactic Lactobacillus GG reduces antibiotic-associated diarrhea in children with respiratory infections: a randomized study. Pediatrics. 1999; 104: e64. PMID: 10545590
24. Shen J, Johnson VM, Sullivan L.M., Jacques PF, Magnani JW, LubitzS A, et al Dietary factors and incident atrial fibrillation: the Framingham Heart Study. Am J Clin Nutr. 2011; 93: 261-266. doi: 10.3945/ajcn.110.001305 PMID: 21106919
25. Martin CR, Walker WA Probiotics: role in pathophysiology and prevention in necrotizing enterocolitis. Semin Perinatol. 2008; 32:127-137. doi: 10.1053/j.semperi.2008.01.006 PMID: 18346537
26. 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. doi: 10.1542/peds.2007-3007 PMID: 18829790
27. Demirel G, Erdeve O, Celik I H., Dilmen U. Saccharomyces boulardii for prevention of necrotizing enterocolitis in preterm infants: a randomized, controlled study. Acta Paediatr. 2013; 102: e560-565. doi: 10.1111/apa.12416 PMID: 24028629
28. 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; 147:192-196. doi: 10.1016/j.jpeds.2005.03.054 PMID: 16126048
29. 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. PMID: 15629973
30. 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. doi: 10.1542/peds.2007-3007 PMID: 18829790
31. Penders J, Thijs C, Vink C., Stelma FF, Snijders B, Kummeling I, et al Factors influencing the composition of the intestinal microbiotain early infancy. Pediatrics. 2006; 118: 511-521. doi: 10.1542/peds.2005-2824 PMID: 16882802
32. 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: 434-439. doi: 10.1038/ejcn.2010.278 PMID: 21245887
33. 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; 89:1033-1036. doi: 10.1016/j.earlhumdev.2013.08.013 PMID: 24041815
34. Demirel G, Celik IH, Erdeve O, Saygan S., Dilmen U, Canpolat FE. Prophylactic Saccharomyces boulardii versus nystatin for the prevention of fungal colonization and invasive fungal infection in premature infants. Eur J Pediatr. 2013; 172:1321-1326. doi: 10.1007/s00431-013-2041-4 PMID: 23703468
35. Li H, Handsaker B, Wysoker A., Fennell T, Ruan J, Homer N., et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25: 2078-2079. doi: 10.1093/bioinformatics/btp352 PMID: 19505943
36. Lab H. FASTX Toolkit [Internet]. Available: http://hannonlab.cshl.edu/fastxtoolkit/
37. Schloss PD, Westcott SL, Ryabin T, Hall J.R., Hartmann M., Hollister EB, et al. Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009; 75: 7537-7541. doi: 10.1128/AEM.01541-09 PMID: 19801464
38. Edgar RC, Haas BJ, Clemente J.C., Quince C., Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-2200. doi: 10.1093/bioinformatics/btr381 PMID: 21700674
39. Parks DH, Tyson GW, Hugenholtz P, Beiko RG STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014; 30: 3123-3124. doi: 10.1093/bioinformatics/btu494 PMID: 25061070
40. Wickham H. ggplot2: Elegant Graphics for Data Analysis. 1st ed. 2009. Corr. 3rd printing 2010 edition. New York: Springer; 2010.
41. Huson DH, Mitra S, Ruscheweyh H-J, Weber N, Schuster SC Integrative analysis of environmental sequences using MEGAN4. Genome Res. 2011; 21:1552-1560. doi: 10.1101/gr.120618.111 PMID: 21690186
42. Asnicar F, Weingart G, Tickle T.L., Huttenhower C., Segata N. Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ. 2015; 3: e1029. doi: 10.7717/peerj.1029 PMID: 26157614
43. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995; 57: 289-300.
44. Faul F, Erdfelder E, Lang A-G, Buchner A. GPower 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007; 39:175-191. PMID: 17695343
45. Brooks JP, Edwards DJ, Harwich M.D., Rivera MC, Fettweis JM, Serrano MG, et al The truth about metagenomics: quantifying and counteracting bias in 16S rRNA studies. BMC Microbiology. 2015; 15: 66. doi: 10.1186/s12866-015-0351-6 PMID: 25880246
46. Walker AW, Martin JC, Scott P, Parkhill J., Flint HJ, Scott KP. 16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice. Microbiome. 2015; 3: 26. doi: 10.1186/s40168-015-0087-4 PMID: 26120470
47. Nelson MC, Morrison HG, Benjamino J, Grim S.L., Graf J. Analysis, optimization and verification of Illumina-generated 16S rRNA gene amplicon surveys. PLoSONE. 2014; 9: e94249. doi: 10.1371/journal.pone.0094249 PMID: 24722003
48. La Rosa P.S., Warner BB, Zhou Y, Weinstock G.M., Sodergren E., Hall-Moore CM, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci USA. 2014; 111: 12522-12527. doi: 10.1073/pnas.1409497111 PMID: 25114261
49. Bäckhed F., Roswall J, Peng Y., Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015; 17: 690-703. doi: 10.1016/j.chom.2015.04.004 PMID: 25974306
50. Abrahamsson TR, Jakobsson HE, Andersson A.F., Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2014; 44: 842-850. doi: 10.1111/cea.12253 PMID: 24330256
51. Storrø O, Avershina E, Rudi K. Diversity of intestinal microbiota in infancy and the risk of allergic disease in childhood. CurrOpin Allergy Clin Immunol. 2013; 13: 257-262. doi: 10.1097/ACI.0b013e328360968b PMID: 23549152
52. Mizrahi-Man O., Davenport ER, Gilad Y. Taxonomic classification of bacterial 16S rRNA genes using short sequencing reads: evaluation of effective study designs. PLoSONE. 2013; 8: e53608. doi: 10.1371/journal.pone.0053608 PMID: 23308262
53. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoSONE. 2013; 8: e61217. doi: 10.1371/journal.pone.0061217 PMID: 23630581
54. Dominguez-Bello M.G., Costello EK, Contreras M, Magris M., Hidalgo G, Fierer N, et al Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010; 107:11971-11975. doi: 10.1073/pnas.1002601107 PMID: 20566857
55. Arboleya S, Sánchez B, Milani C., Duranti S, Solís G, Fernández N, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015; 166: 538-544. doi: 10. 1016/j.jpeds.2014.09.041 PMID: 25444008
56. Jakobsson HE, Abrahamsson TR, Jenmalm M.C., Harris K., Quince C, Jernberg C, et al Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014; 63: 559-566. doi: 10.1136/gutjnl-2012-303249 PMID: 23926244
57. Ling Z, Li Z, Liu X., Cheng Y, Luo Y, Tong X., et al. Altered fecal microbiota composition associated with food allergy in infants. Appl Environ Microbiol. 2014; 80: 2546-2554. doi: 10.1128/AEM.00003-14 PMID: 24532064
58. Abrahamsson TR, Jakobsson HE, Andersson A.F., Björkstén B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2012; 129: 434-440, 440.e1-2. doi: 10.1016/j.jaci.2011.10.025 PMID: 22153774
59. Guibas GV, Moschonis G, Xepapadaki P., Roumpedaki E, Androutsos O, Manios Y., et al. Conception via in vitro fertilization and delivery by Caesarean section are associated with paediatric asthma incidence. Clin Exp Allergy. 2013; 43:1058-1066. doi: 10.1111/cea.12152 PMID: 23957341
60. Neu J. Probiotics and necrotizing enterocolitis. Clin Perinatol. 2014; 41: 967-978. doi: 10.1016/j.clp.2014.08.014 PMID: 25459784
61. Arboleya S, Ang L, Margolles A., Yiyuan L, Dongya Z, Liang X., et al. Deep 16S rRNA metagenomics and quantitative PCR analyses of the premature infant fecal microbiota. Anaerobe. 2012; 18: 378-380. doi: 10.1016/j.anaerobe.2012.04.013 PMID: 22579986
62. Arboleya S, Binetti A, Salazar N., Fernández N, Solís G, Hernández-Barranco A, et al. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol. 2012; 79: 763-772. doi: 10.1111/j.1574-6941.2011.01261.x PMID: 22126419
63. Rougé C, Goldenberg O, Ferraris L, Berger B, Rochat F, Legrand A, et al. Investigation of the intestinal microbiota in preterm infants using different methods. Anaerobe. 2010; 16: 362-370. doi: 10.1016/j.anaerobe.2010.06.002 PMID: 20541022
64. White JR, Nagarajan N, Pop M. Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoSComput Biol. 2009; 5: e1000352. doi: 10.1371/journal.pcbi.1000352 PMID: 19360128
65. Buts J-P, De Keyser N. Transduction pathways regulating the trophic effects of Saccharomyces boulardii in rat intestinal mucosa. Scand J Gastroenterol. 2010; 45:175-185. doi: 10.3109/00365520903453141 PMID: 19958054