Impact of prematurity and perinatal antibiotics on the developing intestinal microbiota: A functional inference study

International Journal of Molecular Sciences

Volumn 17, Issue 5, 2016, Pages

  Arboleya, Silvia ^a   Sánchez, Borja ^a   Solís, Gonzalo ^b   Fernández, Nuria ^c   Suárez, Marta ^b   Hernández Barranco, Ana M ^a   Milani, Christian ^d   Margolles, Abelardo ^a   De Los Reyes Gavilán, Clara G ^a   Ventura, Marco ^d   Gueimonde, Miguel ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

^b HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^c HOSPITAL DE CABUEÑES   (Spain)

^d UNIVERSITY OF PARMA   (Italy)

Author keywords

Antibiotics; Infants; Intestinal microbiota; Microbiome; Preterm

Indexed keywords

ANTIBIOTIC AGENT; RNA 16S; SHORT CHAIN FATTY ACID; ACETIC ACID DERIVATIVE; ANTIINFECTIVE AGENT; BUTYRIC ACID DERIVATIVE; PROPIONIC ACID DERIVATIVE; VOLATILE FATTY ACID;

ACTINOBACTERIA; ARTICLE; BACTEROIDETES; CLINICAL ARTICLE; FECES MICROFLORA; FIRMICUTES; GAS CHROMATOGRAPHY; HUMAN; INTESTINE FLORA; INTRAPARTUM CARE; MASS SPECTROMETRY; MICROBIAL COLONIZATION; NEWBORN; NONHUMAN; PERINATAL DRUG EXPOSURE; PREMATURITY; PROTEOBACTERIA; VERY LOW BIRTH WEIGHT; BREAST FEEDING; CHEMISTRY; DRUG EFFECTS; FECES; INTESTINE; MASS FRAGMENTOGRAPHY; MICROBIOLOGY; MICROFLORA;

ACETATES; ANTI-BACTERIAL AGENTS; BREAST FEEDING; BUTYRATES; FATTY ACIDS, VOLATILE; FECES; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; INTESTINES; MICROBIOTA; PROPIONATES;

EID: 85013073488     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17050649     Document Type: Article

References (53)

1. Turnbaugh, P.J.; Hamady, M.; Yatsunenko, T.; Cantarel, B.L.; Duncan, A.; Ley, R.E.; Sogin, M.L.; Jones, W.J.; Roe, B.A.; Affourtit, J.P.; et al. A core gut microbiome in obese and lean twins. Nature 2009, 457, 480-484
2. Qin, J.; Li, R.; Raes, J.; Arumugam, M.; Burgdorf, K.S.; Manichanh, C.; Nielsen, T.; Pons, N.; Levenez, F.; Yamada, T.; et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464, 59-65
3. Arumugan, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D.R.; Fernandes, G.R.; Tap, J.; Bruls, T.; Batto, J.M.; et al. Enterotypes of the human gut microbiome. Nature 2011, 473, 174-180
4. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486, 207-214.
5. Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; et al. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222-227
6. Karlsson, F.H.; Tremaroli, V.; Nookaew, I.; Bergstrom, G.; Behre, C.J.; Fagerberg, B.; Nielsen, J.; Bäckhed, F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 2013, 498, 99-103
7. Sommer, F.; Bäckhed, F. The gut microbiota-Masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11, 227-238
8. Donaldson, G.P.; Lee, S.N.; Mazmanian, S.K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 2016, 14, 20-32
9. Matamoros, S.; Gras-Leguen, C.; Le Vacon, F.; Potel, G.; de La Cochetiere, M.F. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 2013, 21, 167-173
10. Sim, K.; Powel, E.; Shaw, A.G.; McClure, Z.; Bangham, M.; Kroll, J.S. The neonatal gastrointestinal microbiota: The foundation of future health? Arch. Dis. Child. Fetal Neonatal Ed. 2013, 98, F362-F364
11. Hansen, C.H.; Nielsen, D.S.; Kverka, M.; Zakostelska, Z.; Klimesova, K.; Hudcovic, T.; Tlaskalova-Hogenova, H.; Hansen, A.K. Patterns of early gut microbiota colonization shape future immune responses of the host. PLoS ONE 2012, 7, e34043
12. Olszak, T.; An, D.; Zeissig, S.; Vera, M.P.; Richter, J.; Franke, A.; Glickman, J.N.; Siebert, R.; Baron, R.M.; Kasper, D.L.; et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012, 336, 489-493
13. Cox, L.M.; Yamanishi, S.; Sohn, J.; Alekseyenko, A.V.; Leung, J.M.; Cho, I.; Kim, S.G.; Li, H.; Gao, Z.; Mahana, D.; et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 2014, 158, 705-721
14. Borre, Y.E.; O’Keeffe, G.W.; Clarke, G.; Stanton, C.; Dinan, T.G.; Cryan, J.F. Microbiota and neurodevelopmental windows: Implications for brain disorders. Trends Mol. Med. 2014, 20, 509-518
15. Faa, G.; Gerosa, C.; Fanni, D.; Nemolato, S.; van Eyken, P.; Fanos, V. Factors influencing the development of a personal tailored microbiota in the neonate, with particular emphasis on antibiotic therapy. J. Matern. Fetal Neonatal Med. 2013, 26, 35-43
16. Bäckhed, F.; Roswall, J.; Peng, Y.; Feng, Q.; Jia, H.; Kovatcheva-Datchary, P.; Li, Y.; Xia, Y.; Xie, H.; Zhong, H.; et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 2015, 17, 690-703
17. Del Chierico, F.; Vernocchi, P.; Petruca, A.; Paci, P.; Fuentes, S.; Pratico, G.; Capuani, G.; Masotti, A.; Reddel, S.; Russo, A.; et al. Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PLoS ONE 2015, 10, e0137347.
18. Jakobsson, H.E.; Abrahamsson, T.R.; Jenmalm, M.C.; Harris, K.; Quince, C.; Jernberg, C.; Björkstén, B.; Engstrand, L.; Andersson, A.F. Decreased gut microbiota diversity, delayed Bacteroidetes colonization and reduced Th1 responses in infants delivered by caesarean section. Gut 2014, 63, 559-566
19. Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. 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
20. Dominguez-Bello, M.G.; de Jesus-Laboy, K.M.; Shen, N.; Cox, L.M.; Amir, A.; Gonzalez, A.; Bokullich, N.A.; Song, S.J.; Hoashi, M.; Rivera-Viñas, J.I.; et al. Partial restoration of the microbiota of caesarean-born infants via vaginal microbial transfer. Nat. Med. 2016, 22, 250-253
21. Strunk, T.; Currie, A.; Richmond, P.; Simmer, K.; Burgner, D. Innate immunity in human newborn infants: Prematurity means more than immaturity. J. Matern. Fetal Neonatal Med. 2011, 24, 25-31
22. Arboleya, S.; Sánchez, B.; Milani, C.; Duranti, S.; Solís, G.; Fernández, N.; de los Reyes-Gavilán, C.G.; Ventura, M.; Margolles, A.; Gueimonde, M. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J. Pediatr. 2015, 166, 538-544
23. Wang, Y.; Hoenig, J.D.; Malin, K.J.; Qamar, S.; Petrof, E.O.; Sun, J.; Antonopoulos, D.A.; Chang, E.B.; Claud, E.C. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J. 2009, 3, 944-954
24. Arboleya, S.; Binetti, A.; Salazar, N.; Fernández, N.; Solís, G.; Hernández-Barranco, A.; Margolles, A.; de los Reyes-Gavilán, C.G.; Gueimonde, M. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol. Ecol. 2012, 79, 763-772
25. Mshvildadze, M.; Neu, J.; Shuster, J.; Theriaque, D.; Li, N.; Mai, W. Intestinal microbial ecology in premature infants assessed by non-culture-based techniques. J. Pediatr. 2010, 156, 20-25
26. Arboleya, S.; Solís, G.; Fernández, N.; de los Reyes-Gavilán, C.G.; Gueimonde, M. Facultative to strict anaerobes ratio in the preterm infant microbiota: A target for intervention? Gut Microbes 2012, 3, 583-588
27. Barrett, E.; Kerr, C.; Murphy, K.; O’Sullivan, O.; Ryan, C.A.; Dempsey, E.M.; Murphy, B.P.; O’Toole, P.W.; Cotter, P.D.; Fitzgerald, G.F.; et al. The individual-specific and diverse nature of the preterm infant microbiota. Arch. Dis. Child. Fetal Neonatal Ed. 2013, 98, F334-F340
28. Morrow, A.L.; Lagomarcino, A.J.; Schibler, K.R.; Taft, D.H.; Yo, Z.; Wang, B.; Altaye, M.; Wagner, M.; Gevers, D.; Ward, D.V.; et al. Early microbial and metabolomic signatures predict later onset of necrotizing enterocolitis in preterm infants. Microbiome 2013, 1
29. Aloisio, I.; Quagliariello, A.; de Fanti, S.; Luiselli, D.; de Filippo, C.; Albanese, D.; Corvaglia, L.T.; Faldella, G.; di Gioia, D. Evaluation of the effects of intrapartum antibiotic prophylaxix on newborn intestinal microbiota using a sequencing approach targeted to multi hypervariate 16S rDNA regions. Appl. Microbiol. Biotechnol. 2016
30. Koenig, J.E.; Spor, A.; Scalfone, N.; Fricker, A.D.; Stombaugh, J.; Knight, R.; Angenent, L.T.; Ley, R.E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA 2011, 108, 4578-4585
31. Arboleya, S.; Ang, L.; Margolles, A.; Yiyuan, L.; Dongya, Z.; Liang, X.; Solís, G.; Fernández, N.; de los Reyes-Gavilán, C.G.; Gueimonde, M. Deep 16S rRNA metagenomics and quantitative PCR analyses of the premature infant fecal microbiota. Anaerobe 2012, 18, 378-380
32. Stewart, C.J.; Marrs, E.C.; Nelson, A.; Lanyon, C.; Perry, J.D.; Embleton, N.D.; Cummings, S.P.; Berrington, J.E. Development of the preterm gut microbiome in twins at risk of necrotising enterocolitis and sepsis. PLoS ONE 2013, 8, e73465
33. Avershina, E.; Storro, O.; Oien, T.; Johnsen, R.; Pope, P.; Rudi, K. Major fecal microbiota shifts in composition and diversity with age in a geographically restricted cohort of mothers and their children. FEMS Microbiol. Ecol. 2014, 87, 280-290
34. Morgan, X.C.; Tickle, T.L.; Sokol, H.; Gevers, D.; Devaney, K.L.; Ward, D.V.; Reyes, J.A.; Shah, S.A.; LeLeiko, N.; Snapper, S.B.; et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012, 13, R79
35. Tanaka, S.; Kobayashi, T.; Songjinda, P.; Tateyama, A.; Tsubouchi, M.; Kiyohara, C.; Shirakawa, T.; Sonomoto, K.; Nakayama, J. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. FEMS Immunol. Med. Microbiol. 2009, 56, 80-87
36. Fallani, M.; Young, D.; Scott, J.; Norin, E.; Amarri, S.; Adam, R.; Aguilera, M.; Khanna, S.; Gil, A.; Edwards, C.A.; et al. Intestinal microbiota of 6-week-old infants across Europe: Geographic influence beyond delivery mode, breast-feeding and antibiotics. J. Pediatr. Gastroenterol. Nutr. 2010, 51, 77-84
37. Fouhy, F.; Guinane, C.M.; Hussey, S.; Wall, R.; Ryan, C.A.; Dempsey, E.M.; Murphy, B.; Ross, R.P.; Fitzgerald, G.F.; Stanton, C.; et al. High-Throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicilin and gentamicin. Antimicrob. Agents Chemother. 2012, 56, 5811-5820
38. Penders, J.; Thijs, C.; Vink, C.; Stelma, F.F.; Snijders, B.; Kummeling, I.; van den Brandt, P.A.; Stobberingh, E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 2006, 118, 511-521
39. Azad, M.B.; Konya, T.; Persaud, R.R.; Guttman, D.S.; Chari, R.S.; Field, C.J.; Sears, M.R.; Mandhane, P.J.; Turvey, S.E.; Subbarao, P.; et al. Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: A prospective cohort study. BJOG Int. J. Obstet. Gynaecol. 2015
40. Russell, S.L.; Gold, M.J.; Hartmann, M.; Willing, B.P.; Thorson, L.; Wlodarska, M.; Gill, N.; Blanchet, M.R.; Mohn, W.W.; McNagny, K.M.; et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 2012, 13, 440-447
41. Chu, S.; Yu, H.; Chen, Y.; Chen, Q.; Wang, B.; Zhang, J. Periconceptional and gestational exposure to antibiotics and childhood asthma. PLoS ONE 2015, 10, e0140443
42. Van Dyke, M.K.; Phares, C.R.; Lynfield, R.; Thomas, A.R.; Arnold, K.E.; Craig, A.S.; Mohle-Boetani, J.; Gershman, K.; Schaffner, W.; Petit, S.; et al. Evaluation of universal antenatal screening for group B streptococcus. N. Engl. J. Med. 2009, 360, 2626-2636
43. Kenyon, S.; Boulvain, M.; Neilson, J.P. Antibiotics for preterm rupture of membranes. Cochrane Database Syst. Rev. 2010, 8, CD001058
44. Allen, V.M.; Yudin, M.H.; Bouchard, C.; Boucher, M.; Caddy, S.; Castillo, E.; Money, D.M.; Murphy, K.E.; Ogilvie, G.; Paquet, C.; et al. Management of group B streptococcal bacteriuria in pregnancy. J. Obstet. Gynaecol. Can. 2012, 34, 482-486
45. King, J.F.; Flenady, V.; Murray, L. Prophylactic antibiotics for inhibiting preterm labour with intact membranes. Cochrane Database Syst. Rev. 2002, 4, CD000246
46. Russell, B.A.R.; Murch, S.H. Could peripartum antibiotics have delayed health consequences for the infant? BJOG Int. J. Obstet. Gynaecol. 2006, 113, 758-765
47. 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
48. Milani, C.; Hevia, A.; Foroni, E.; Duranti, S.; Turroni, F.; Lugli, G.A.; Sanchez, B.; Martín, R.; Gueimonde, M.; van Sinderen, D.; et al. Assessing the fecal microbiota: An optimized Ion Torrent 16S rRNA gene-based analysis protocol. PLoS ONE 2013, 8, e68739
49. Langille, M.G.; Zaneveld, J.; Caporaso, J.G.; McDonald, D.; Knights, D.; Reyes, J.A.; Clemente, J.C.; Burkepile, D.E.; Vega Thurber, R.L.; Knight, R.; et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31, 814-821
50. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335-336
51. McDonald, D.; Clemente, J.C.; Kuczynski, J.; Rideout, J.R.; Stombaugh, J.; Wendel, D.; Wilke, A.; Huse, S.; Hufnagle, J.; Meyer, F.; et al. The Biological Observation Matrix (BIOM) format or: How I learned to stop worrying and love the ome-ome. Gigascience 2012, 1, 7
52. Parks, D.H.; Beiko, R.G. Identifying biologically relevant differences between metagenomic communities. Bioinformatics 2010, 26, 715-721
53. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 1995, 57, 289-300