Impact of intrapartum antibiotic prophylaxis on the oral and fecal bacteriomes of children in the first week of life.
Humans
Antibiotic Prophylaxis
/ methods
Feces
/ microbiology
Female
Infant, Newborn
Pregnancy
Mouth
/ microbiology
Anti-Bacterial Agents
/ administration & dosage
Adult
RNA, Ribosomal, 16S
/ genetics
Cesarean Section
Male
Gastrointestinal Microbiome
/ drug effects
Meconium
/ microbiology
Delivery, Obstetric
Bacteria
/ genetics
16S rRNA
Antibiotics
Diversity
Infant
Microbiome
Mother
Next-generation sequencing
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
06 Aug 2024
06 Aug 2024
Historique:
received:
15
02
2024
accepted:
30
07
2024
medline:
7
8
2024
pubmed:
7
8
2024
entrez:
6
8
2024
Statut:
epublish
Résumé
Intrapartum antibiotic prophylaxis (IAP) is commonly used during C-section delivery and in Group B Streptococcus-positive women before vaginal delivery. Here, we primarily aimed to investigate the effect of IAP on the neonatal oral and fecal bacteriomes in the first week of life. In this preliminary study, maternal and neonatal oral swabs and neonatal fecal (meconium and transitional stool) swabs were selected from a pool of samples from healthy mother-neonate pairs participating in the pilot phase of CELSPAC: TNG during their hospital stay. The DNA was extracted and bacteriome profiles were determined by 16S rRNA amplicon sequencing (Illumina). In the final dataset, 33 mother-neonate pairs were exposed to antibiotics during C-section or vaginal delivery (cases; +IAP) and the vaginal delivery without IAP (controls, -IAP) took place in 33 mother-neonate pairs. Differences in alpha diversity (Shannon index, p=0.01) and bacterial composition (PERMANOVA, p<0.05) between the +IAP and -IAP groups were detected only in neonatal oral samples collected ≤48 h after birth. No significant differences between meconium bacteriomes of the +IAP and -IAP groups were observed (p>0.05). However, the IAP was associated with decreased alpha diversity (number of amplicon sequence variants, p<0.001), decreased relative abundances of the genera Bacteroides and Bifidobacterium, and increased relative abundances of genera Enterococcus and Rothia (q<0.01 for all of them) in transitional stool samples. The findings of this study suggest that exposure to IAP may significantly influence the early development of the neonatal oral and gut microbiomes. IAP affected the neonatal oral bacteriome in the first two days after birth as well as the neonatal fecal bacteriome in transitional stool samples. In addition, it highlights the necessity for further investigation into the potential long-term health impacts on children.
Identifiants
pubmed: 39107353
doi: 10.1038/s41598-024-68953-z
pii: 10.1038/s41598-024-68953-z
doi:
Substances chimiques
Anti-Bacterial Agents
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18163Subventions
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : 65269705
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LM2023069
Organisme : Horizon 2020 Framework Programme
ID : 857560
Organisme : HORIZON EUROPE European Research Council
ID : No 101136566
Informations de copyright
© 2024. The Author(s).
Références
Shao, Y. et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 574, 117–21 (2019).
pubmed: 31534227
pmcid: 6894937
doi: 10.1038/s41586-019-1560-1
Mueller, N. T., Bakacs, E., Combellick, J., Grigoryan, Z. & Dominguez-Bello, M. G. The infant microbiome development: Mom matters. Trends Mol. Med. 21, 109–17 (2015).
pubmed: 25578246
doi: 10.1016/j.molmed.2014.12.002
Grech, A. et al. Maternal exposures and the infant gut microbiome: A systematic review with meta-analysis. Gut Microbes 13, 1–30 (2021).
pubmed: 33978558
doi: 10.1080/19490976.2021.1897210
Bäckhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703 (2015).
pubmed: 25974306
doi: 10.1016/j.chom.2015.04.004
Rutayisire, E., Huang, K., Liu, Y. & Tao, F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: A systematic review. BMC Gastroenterol. 16, 86 (2016).
pubmed: 27475754
pmcid: 4967522
doi: 10.1186/s12876-016-0498-0
Shaterian, N., Abdi, F., Ghavidel, N. & Alidost, F. Role of cesarean section in the development of neonatal gut microbiota: A systematic review. Open Med. Wars Pol. 16, 624–39 (2021).
doi: 10.1515/med-2021-0270
Pivrncova, E., Kotaskova, I. & Thon, V. Neonatal diet and gut microbiome development after C-section during the first three months after birth: A systematic review. Front. Nutr. 9, 941549 (2022).
pubmed: 35967823
pmcid: 9364824
doi: 10.3389/fnut.2022.941549
Nardi, G. M. et al. Maternal and neonatal oral microbiome developmental patterns and correlated factors: A systematic review—does the apple fall close to the tree?. Int. J. Environ. Res. Public Health 18, 5569 (2021).
pubmed: 34071058
pmcid: 8197112
doi: 10.3390/ijerph18115569
Sandall, J. et al. Short-term and long-term effects of caesarean section on the health of women and children. Lancet (London, England) 392, 1349–57 (2018).
pubmed: 30322585
doi: 10.1016/S0140-6736(18)31930-5
Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U. S. A. 107, 11971–5 (2010).
pubmed: 20566857
pmcid: 2900693
doi: 10.1073/pnas.1002601107
Bokulich, N. A. et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med. https://doi.org/10.1126/scitranslmed.aad7121 (2016).
doi: 10.1126/scitranslmed.aad7121
pubmed: 27306664
pmcid: 5308924
Nogacka, A. et al. Impact of intrapartum antimicrobial prophylaxis upon the intestinal microbiota and the prevalence of antibiotic resistance genes in vaginally delivered full-term neonates. Microbiome 5, 93 (2017).
pubmed: 28789705
pmcid: 5549288
doi: 10.1186/s40168-017-0313-3
Money, D., Allen, V. M., Infectious Diseases Committee. The prevention of early-onset neonatal group B streptococcal disease. J. Obstet. Gynaecol. Can. JOGC 35, 939–948 (2013).
pubmed: 24165063
doi: 10.1016/S1701-2163(15)30818-5
Betran, A. P., Ye, J., Moller, A.-B., Souza, J. P. & Zhang, J. Trends and projections of caesarean section rates: Global and regional estimates. BMJ Glob. Health 6, e005671 (2021).
pubmed: 34130991
pmcid: 8208001
doi: 10.1136/bmjgh-2021-005671
Seale, A. C. et al. Estimates of the burden of group b streptococcal disease worldwide for pregnant women, stillbirths, and children. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 65(Suppl 2), S200-19 (2017).
doi: 10.1093/cid/cix664
Trijbels-Smeulders, M. et al. Epidemiology of neonatal group B streptococcal disease in the Netherlands before and after introduction of guidelines for prevention. Arch. Dis. Child. Fetal Neonatal Ed. 92, F271-276 (2007).
pubmed: 17227807
pmcid: 2675425
doi: 10.1136/adc.2005.088799
Schrag, S. J. & Verani, J. R. Intrapartum antibiotic prophylaxis for the prevention of perinatal group B streptococcal disease: Experience in the United States and implications for a potential group B streptococcal vaccine. Vaccine 31(Suppl 4), D20-26 (2013).
pubmed: 23219695
doi: 10.1016/j.vaccine.2012.11.056
Zhu, Y. & Lin, X.-Z. Updates in prevention policies of early-onset group B streptococcal infection in newborns. Pediatr. Neonatol. 62, 465–75 (2021).
pubmed: 34099416
doi: 10.1016/j.pedneo.2021.05.007
Hasperhoven, G., Al-Nasiry, S., Bekker, V., Villamor, E. & Kramer, B. Universal screening versus risk-based protocols for antibiotic prophylaxis during childbirth to prevent early-onset group B streptococcal disease: A systematic review and meta-analysis. BJOG Int. J. Obstet. Gynaecol. 127, 680–91 (2020).
doi: 10.1111/1471-0528.16085
Van Dyke, M. K. et al. Evaluation of universal antenatal screening for group B streptococcus. N. Engl. J. Med. 360, 2626–36 (2009).
pubmed: 19535801
doi: 10.1056/NEJMoa0806820
Stearns, J. C. et al. Intrapartum antibiotics for GBS prophylaxis alter colonization patterns in the early infant gut microbiome of low risk infants. Sci. Rep. 7, 16527 (2017).
pubmed: 29184093
pmcid: 5705725
doi: 10.1038/s41598-017-16606-9
Zimmermann, P. & Curtis, N. Effect of intrapartum antibiotics on the intestinal microbiota of infants: A systematic review. Arch. Dis. Child. Fetal Neonatal Ed. 105, 201–8 (2020).
pubmed: 31296695
doi: 10.1136/archdischild-2018-316659
Hirsch, A. G. et al. Early life antibiotic use and subsequent diagnosis of food allergy and allergic diseases. Clin. Exp. Allergy J. Br. Soc. Allergy Clin. Immunol. 47, 236–44 (2017).
doi: 10.1111/cea.12807
Kummeling, I. et al. Early life exposure to antibiotics and the subsequent development of eczema, wheeze, and allergic sensitization in the first 2 years of life: The KOALA birth cohort study. Pediatrics 119, e225-31 (2007).
pubmed: 17200248
doi: 10.1542/peds.2006-0896
Azad, M. B., Bridgman, S. L., Becker, A. B. & Kozyrskyj, A. L. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int. J. Obes. 38, 1290–8 (2014).
doi: 10.1038/ijo.2014.119
Gomez Arango, L. et al. Antibiotic treatment at delivery shapes the initial oral microbiome in neonates. Sci. Rep. 7, 43481 (2017).
pubmed: 28240736
pmcid: 5378909
doi: 10.1038/srep43481
Tapiainen, T. et al. Impact of intrapartum and postnatal antibiotics on the gut microbiome and emergence of antimicrobial resistance in infants. Sci. Rep. 9, 10635 (2019).
pubmed: 31337807
pmcid: 6650395
doi: 10.1038/s41598-019-46964-5
Chen, Y. Y. et al. Impact of maternal intrapartum antibiotics, and caesarean section with and without labour on bifidobacterium and other infant gut microbiota. Microorganisms 9, 1847 (2021).
pubmed: 34576741
pmcid: 8467529
doi: 10.3390/microorganisms9091847
Azad, M. 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. 123, 983–93 (2016).
doi: 10.1111/1471-0528.13601
Aloisio, I. et al. Influence of intrapartum antibiotic prophylaxis against group B Streptococcus on the early newborn gut composition and evaluation of the anti-Streptococcus activity of Bifidobacterium strains. Appl. Microbiol. Biotechnol. 98, 6051–60 (2014).
pubmed: 24687755
Zhou, P. et al. Perinatal antibiotic exposure affects the transmission between maternal and neonatal microbiota and is associated with early-onset sepsis. mSphere 5, e00984-19 (2020).
pubmed: 32075882
pmcid: 7031618
doi: 10.1128/mSphere.00984-19
Pavlova, T. et al. Urinary intermediates of tryptophan as indicators of the gut microbial metabolism. Anal. Chim. Acta 987, 72–80 (2017).
pubmed: 28916042
doi: 10.1016/j.aca.2017.08.022
Videnska, P. et al. Stool sampling and DNA isolation kits affect DNA quality and bacterial composition following 16S rRNA gene sequencing using MiSeq Illumina platform. Sci. Rep. 9, 13837 (2019).
pubmed: 31554833
pmcid: 6761292
doi: 10.1038/s41598-019-49520-3
Douglas, C. A. et al. DNA extraction approaches substantially influence the assessment of the human breast milk microbiome. Sci. Rep. 10, 123 (2020).
pubmed: 31924794
pmcid: 6954186
doi: 10.1038/s41598-019-55568-y
Claassen, S. et al. A comparison of the efficiency of five different commercial DNA extraction kits for extraction of DNA from faecal samples. J. Microbiol. Methods 94, 103–10 (2013).
pubmed: 23684993
pmcid: 5809576
doi: 10.1016/j.mimet.2013.05.008
Kotásková, I. et al. Actinotignum schaalii: Relation to concomitants and connection to patients’ conditions in polymicrobial biofilms of urinary tract catheters and urines. Microorganisms 9, 669 (2021).
pubmed: 33807120
pmcid: 8004716
doi: 10.3390/microorganisms9030669
Tourlousse, D. M. et al. Synthetic spike-in standards for high-throughput 16S rRNA gene amplicon sequencing. Nucleic Acids Res. 45, e23 (2017).
pubmed: 27980100
Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108, 4516–22 (2011).
pubmed: 20534432
doi: 10.1073/pnas.1000080107
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–3 (2016).
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Aronesty, E. Comparison of sequencing utility programs. Open Bioinform. J. 7, 1–8 (2013).
doi: 10.2174/1875036201307010001
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–6 (2010).
pubmed: 20383131
pmcid: 3156573
doi: 10.1038/nmeth.f.303
Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590-6 (2013).
pubmed: 23193283
doi: 10.1093/nar/gks1219
Baldassarre, M. E. et al. Duration of meconium passage in preterm and term infants. Arch. Dis. Child. Fetal Neonatal Ed. 95, F74-75 (2010).
pubmed: 20019200
doi: 10.1136/adc.2009.159442
Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226 (2018).
pubmed: 30558668
pmcid: 6298009
doi: 10.1186/s40168-018-0605-2
Pincus, R. & Aitchison, J. The Statistical Analysis of Compositional Data. Biom J. 30, 794–794 (Chapman and Hall, London, New York, 1988).
R: The R Project for Statistical Computing. https://www.r-project.org/ (2023).
Van den Boogaart, K. & Tolosana-Delgado, R. Compositional data analysis with `R’ and the package ‘compositions’. Geol. Soc. 264(1), 119–127 (2006).
Oksanen, J, et al. Vegan: Community Ecology Package. http://cran.r-project.org (2022).
Kassambara, A. & Mundt, F. Factoextra: Extract and visualize the results of multivariate data analyses. https://CRAN.R-project.org/package=factoextra (2020).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).
Murray, M. & Blume, J. FDRestimation: Estimate, Plot, and Summarize False Discovery Rates. https://doi.org/10.12688/f1000research.52999.2 (2022).
Conway, J. & Gehlenborg N. UpSetR: A More Scalable Alternative to Venn and Euler Diagrams for Visualizing Intersecting Sets. https://doi.org/10.1093/bioinformatics/btx364 (2019).
Guo, H. et al. The dynamic communities of oral microbiome in neonates. Front. Microbiol. 13, 1052525 (2022).
pubmed: 36560953
pmcid: 9764626
doi: 10.3389/fmicb.2022.1052525
Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133-145.e5 (2018).
pubmed: 30001516
pmcid: 6716579
doi: 10.1016/j.chom.2018.06.005
Dzidic, M. et al. Oral microbiome development during childhood: An ecological succession influenced by postnatal factors and associated with tooth decay. ISME J. 12, 2292–306 (2018).
pubmed: 29899505
pmcid: 6092374
doi: 10.1038/s41396-018-0204-z
Belizário, J. E. & Napolitano, M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front. Microbiol. 6, 1050 (2015).
pubmed: 26500616
pmcid: 4594012
doi: 10.3389/fmicb.2015.01050
Xiao, J., Fiscella, K. A. & Gill, S. R. Oral microbiome: Possible harbinger for children’s health. Int. J. Oral Sci. 12, 1–13 (2020).
doi: 10.1038/s41368-020-0082-x
Sampaio-Maia, B. & Monteiro-Silva, F. Acquisition and maturation of oral microbiome throughout childhood: An update. Dent. Res. J. 11, 291–301 (2014).
Chu, D. M. et al. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat. Med. 23, 314–26 (2017).
pubmed: 28112736
pmcid: 5345907
doi: 10.1038/nm.4272
Verma, D., Garg, P. K. & Dubey, A. K. Insights into the human oral microbiome. Arch. Microbiol. 200, 525–40 (2018).
pubmed: 29572583
doi: 10.1007/s00203-018-1505-3
Lif Holgerson, P., Harnevik, L., Hernell, O., Tanner, A. C. R. & Johansson, I. Mode of birth delivery affects oral microbiota in infants. J. Dent. Res. 90, 1183–8 (2011).
pubmed: 21828355
pmcid: 3173012
doi: 10.1177/0022034511418973
Dzidic, M. et al. Oral microbiota maturation during the first 7 years of life in relation to allergy development. Allergy 73, 2000–11 (2018).
pubmed: 29602225
doi: 10.1111/all.13449
Boix-Amorós, A., Collado, M. C. & Mira, A. Relationship between milk microbiota, bacterial load, macronutrients, and human cells during lactation. Front. Microbiol. 7, 492 (2016).
pubmed: 27148183
pmcid: 4837678
doi: 10.3389/fmicb.2016.00492
Miyoshi, T. et al. Gemella haemolysans inhibits the growth of the periodontal pathogen Porphyromonas gingivalis. Sci. Rep. 11, 11742 (2021).
pubmed: 34083694
pmcid: 8175725
doi: 10.1038/s41598-021-91267-3
Peng, X. et al. Oral microbiota in human systematic diseases. Int. J. Oral Sci. 14, 1–11 (2022).
doi: 10.1038/s41368-022-00163-7
Li, H. et al. The impacts of delivery mode on infant’s oral microflora. Sci. Rep. 8, 11938 (2018).
pubmed: 30093722
pmcid: 6085361
doi: 10.1038/s41598-018-30397-7
Hurley, E. et al. The microbiota of the mother at birth and its influence on the emerging infant oral microbiota from birth to 1 year of age: A cohort study. J. Oral Microbiol. 11, 1599652 (2019).
pubmed: 32128038
pmcid: 7034431
doi: 10.1080/20002297.2019.1599652
Kennedy, B. et al. Oral microbiota development in early childhood. Sci. Rep. 9, 19025 (2019).
pubmed: 31836727
pmcid: 6911045
doi: 10.1038/s41598-019-54702-0
Dierikx, T. H. et al. The influence of prenatal and intrapartum antibiotics on intestinal microbiota colonisation in infants: A systematic review. J. Infect. 81, 190–204 (2020).
pubmed: 32389786
doi: 10.1016/j.jinf.2020.05.002
Jauréguy, F. et al. Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J. Clin. Microbiol. 42, 5184–8 (2004).
pubmed: 15528713
pmcid: 525278
doi: 10.1128/JCM.42.11.5184-5188.2004
Arboleya, S., Saturio, S. & Gueimonde, M. Impact of intrapartum antibiotics on the developing microbiota: A review. Microbiome Res. Rep. 1, 22 (2022).
pubmed: 38046905
pmcid: 10688785
doi: 10.20517/mrr.2022.04
Imoto, N. et al. Administration of β-lactam antibiotics and delivery method correlate with intestinal abundances of Bifidobacteria and Bacteroides in early infancy, in Japan. Sci. Rep. 11, 6231 (2021).
pubmed: 33737648
pmcid: 7973812
doi: 10.1038/s41598-021-85670-z
Saturio, S. et al. Effect of intrapartum antibiotics prophylaxis on the bifidobacterial establishment within the neonatal gut. Microorganisms 9, 1867 (2021).
pubmed: 34576761
pmcid: 8471514
doi: 10.3390/microorganisms9091867
Corvaglia, L. et al. Influence of intrapartum antibiotic prophylaxis for group B streptococcus on gut microbiota in the first month of life. J. Pediatr. Gastroenterol. Nutr. 62, 304 (2016).
pubmed: 26237371
doi: 10.1097/MPG.0000000000000928
Dierikx, T. et al. Influence of timing of maternal antibiotic administration during caesarean section on infant microbial colonisation: A randomised controlled trial. Gut 71, 1803–11 (2022).
pubmed: 34803023
doi: 10.1136/gutjnl-2021-324767
Mazzola, G. et al. Early gut microbiota perturbations following intrapartum antibiotic prophylaxis to prevent group B streptococcal disease. PLoS ONE 11, e0157527 (2016).
pubmed: 27332552
pmcid: 4917232
doi: 10.1371/journal.pone.0157527