Clinical research

Relationship among maternal gut, vaginal microbiota and microbiota in meconium and vernix caseosa in newborns

  • Jinqian MA ,
  • Pianpian FAN ,
  • Tao ZHENG ,
  • Lin ZHANG ,
  • Yuanzhi CHEN ,
  • Jian SHEN ,
  • Fengxiu OUYANG
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  • 1.Ministry of Education and Shanghai Key Laboratory of Children′s Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
    2.School of Exercise and Health, Shanghai University of Sport, Shanghai 200438, China
    3.Department of Obstetrics and Gynecology, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200092, China
    4.Department of Obstetrics, International Peace Maternity and Child Health Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China
    5.Key Laboratory of Ministry of Education for Systems Biomedicine; Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai 200240, China
OUYANG Fengxiu, E-mail: ouyangfengxiu@xinhuamed.com.cn.

Received date: 2023-06-09

  Accepted date: 2023-12-05

  Online published: 2024-01-28

Supported by

National Key R&D Program of China(2017YFE0124700);National Natural Science Foundation of China(81961128023);“Two-hundred Talents” Program of Shanghai Jiao Tong University School of Medicine(20152518)

Abstract

Objective ·To analyze the diversity and composition of the maternal gut microbiota and vaginal microbiota in late pregnancy, neonatal meconium microbiota and vernix caseosa microbiota, and analyze the similarities, differences and correlations. Methods ·This is a prospective study. Maternal stool samples and vaginal swabs in late-pregnancy, and neonatal meconium samples were collected from 11 mother-infant pairs at Xinhua Hospital, Shanghai Jiao Tong University School of Medicine from August to November 2018; the vernix caseosa from three sites (forehead, axilla, and inguinal crease) and meconium samples were collected from 14 healthy newborns at International Peace Maternity and Child Health Hospital, Shanghai Jiao Tong University School of Medicine in December 2018. All births were vaginal deliveries. The 16S rRNA gene V3?V4 region sequencing was used. The diversity, composition and similarities/differences of the maternal gut microbiota, the vaginal microbiota, and the neonatal meconium microbiota from the 11 mother-infant pairs, as well as the neonatal vernix caseosa microbiota and the meconium microbiota from the 14 newborns were analyzed. Results ·The number of operational taxonomic units (OTUs), ACE index, Chao1 index, and Shannon index of maternal gut microbiota were all higher than those of vaginal microbiota; the ACE indices and the Chao1 indices of the vernix caseosa microbiota at three sites were all higher than those of meconium microbiota (P<0.01). The β diversity varied among the maternal gut microbiota, vaginal microbiota, and neonatal meconium microbiota (P<0.01). The β diversity of neonatal vernix caseosa microbiota from three sites (forehead, axilla, and inguinal crease) was similar, but different from meconium microbiota (P<0.01). At the phylum level, the dominant bacteria were Firmicutes (52.76%) and Bacteroidetes (41.67%) in the maternal gut microbiota, Firmicutes (74.36%) and Actinobacteria (21.25%) in the maternal vaginal microbiota, and Firmicutes (84.22%) and Proteobacteria (8.80%) in the neonatal vernix caseosa microbiota. The dominant bacterium in the neonatal meconium was Proteobacteria in the two batches of samples (81.11% and 88.72%, respectively). At the genus level, the dominant bacteria were Bacteroides (35.42%) and Faecalibacterium (10.12%) in the maternal gut microbiota, Lactobacillus (69.10%) and Bifidobacterium (11.30%) in the vaginal microbiota, and Lactobacillus (79.81%) and Pseudomonas (3.23%) in the vernix caseosa microbiota. The dominant bacterium in the neonatal meconium was Escherichia in the two batches of samples (55.21% and 31.18%, respectively). Conclusion ·The α diversity of maternal gut microbiota is higher than that of vaginal microbiota and neonatal meconium microbiota, and it is higher in neonatal vernix caseosa than that in meconium microbiota. The Firmicutes is the predominant phylum in the maternal late-pregnancy gut microbiota, vaginal microbiota, and neonatal vernix microbiota. Lactobacillus is the predominant genus in both maternal vaginal and neonatal vernix caseosa microbiota. Proteobacteria in phylum and Escherichia in genus are predominant in meconium microbiota. The microbiota composition is similar in vernix caseosa at different body sites, but there are differences between the vernix caseosa microbiota and meconium microbiota.

Cite this article

Jinqian MA , Pianpian FAN , Tao ZHENG , Lin ZHANG , Yuanzhi CHEN , Jian SHEN , Fengxiu OUYANG . Relationship among maternal gut, vaginal microbiota and microbiota in meconium and vernix caseosa in newborns[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2024 , 44(1) : 50 -63 . DOI: 10.3969/j.issn.1674-8115.2024.01.006

References

1 LI D T, WANG P, WANG P P, et al. The gut microbiota: a treasure for human health[J]. Biotechnol Adv, 2016, 34(7): 1210-1224.
2 WAMPACH L, HEINTZ-BUSCHART A, FRITZ J V, et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential[J]. Nat Commun, 2018, 9(1): 5091.
3 ARRIETA M C, ARéVALO A, STIEMSMA L, et al. Associations between infant fungal and bacterial dysbiosis and childhood atopic wheeze in a nonindustrialized setting[J]. J Allergy Clin Immunol, 2018, 142(2): 424-434.e10.
4 RAUTAVA S, LUOTO R, SALMINEN S, et al. Microbial contact during pregnancy, intestinal colonization and human disease[J]. Nat Rev Gastroenterol Hepatol, 2012, 9(10): 565-576.
5 KRONMAN M P, ZAOUTIS T E, HAYNES K, et al. Antibiotic exposure and IBD development among children: a population-based cohort study[J]. Pediatrics, 2012, 130(4): e794-e803.
6 STOUT M J, CONLON B, LANDEAU M, et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations[J]. Am J Obstet Gynecol, 2013, 208(3): 226.e1-226.e7.
7 MOREIRA L B, SILVA C B D, GERALDO-MARTINS V R, et al. Presence of Streptococcus mutans and interleukin-6 and -10 in amniotic fluid[J]. J Matern Fetal Neonatal Med, 2022, 35(25): 9463-9469.
8 WITT R G, BLAIR L, FRASCOLI M, et al. Detection of microbial cell-free DNA in maternal and umbilical cord plasma in patients with chorioamnionitis using next generation sequencing[J]. PLoS One, 2020, 15(4): e0231239.
9 MAKINO H, KUSHIRO A, ISHIKAWA E, et al. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota[J]. PLoS One, 2013, 8(11): e78331.
10 ARBOLEYA S, SáNCHEZ B, MILANI C, et al. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics[J]. J Pediatr, 2015, 166(3): 538-544.
11 FALLANI M, YOUNG D, SCOTT J, et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics[J]. J Pediatr Gastroenterol Nutr, 2010, 51(1): 77-84.
12 VISSCHER M O, NARENDRAN V, PICKENS W L, et al. Vernix caseosa in neonatal adaptation[J]. J Perinatol, 2005, 25(7): 440-446.
13 ECHARRI P P, GRACIá C M, BERRUEZO G R, et al. Assessment of intestinal microbiota of full-term breast-fed infants from two different geographical locations[J]. Early Hum Dev, 2011, 87(7): 511-513.
14 TAPIAINEN T, PAALANNE N, TEJESVI M V, et al. Maternal influence on the fetal microbiome in a population-based study of the first-pass meconium[J]. Pediatr Res, 2018, 84(3): 371-379.
15 STINSON L F, BOYCE M C, PAYNE M S, et al. The not-so-sterile womb: evidence that the human fetus is exposed to bacteria prior to birth[J]. Front Microbiol, 2019, 10: 1124.
16 KLOPP J, FERRETTI P, MEYER C U, et al. Meconium microbiome of very preterm infants across Germany[J]. mSphere, 2022, 7(1): e0080821.
17 TANG N, LUO Z C, ZHANG L, et al. The association between gestational diabetes and microbiota in placenta and cord blood[J]. Front Endocrinol, 2020, 11: 550319.
18 MITCHELL C M, HAICK A, NKWOPARA E, et al. Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women[J]. Am J Obstet Gynecol, 2015, 212(5): 611.e1-611.e9.
19 THEIS K R, ROMERO R, WINTERS A D, et al. Does the human placenta delivered at term have a microbiota? Results of cultivation, quantitative real-time PCR, 16S rRNA gene sequencing, and metagenomics[J]. Am J Obstet Gynecol, 2019, 220(3): 267.e1-267.e39.
20 STERPU I, FRANSSON E, HUGERTH L W, et al. No evidence for a placental microbiome in human pregnancies at term[J]. Am J Obstet Gynecol, 2021, 224(3): 296.e1-296.e23.
21 FERRETTI P, PASOLLI E, TETT A, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome[J]. Cell Host Microbe, 2018, 24(1): 133-145.e5.
22 ROBERTSON R C, MANGES A R, FINLAY B B, et al. The human microbiome and child growth: first 1000 days and beyond[J]. Trends Microbiol, 2019, 27(2): 131-147.
23 WAMPACH L, HEINTZ-BUSCHART A, HOGAN A, et al. Colonization and succession within the human gut microbiome by Archaea, bacteria, and microeukaryotes during the first year of life[J]. Front Microbiol, 2017, 8: 738.
24 MILLER J L, SONIES B C, MACEDONIA C. Emergence of oropharyngeal, laryngeal and swallowing activity in the developing fetal upper aerodigestive tract: an ultrasound evaluation[J]. Early Hum Dev, 2003, 71(1): 61-87.
25 MILANI C, DURANTI S, BOTTACINI F, et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota[J]. Microbiol Mol Biol Rev, 2017, 81(4): e00036-e00017.
26 JIMéNEZ E, FERNáNDEZ L, MARíN M L, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section[J]. Curr Microbiol, 2005, 51(4): 270-274.
27 LIU C J, LIANG X, NIU Z Y, et al. Is the delivery mode a critical factor for the microbial communities in the meconium?[J]. EBioMedicine, 2019, 49: 354-363.
28 GOMEZ DE AGüERO M, GANAL-VONARBURG S C, FUHRER T, et al. The maternal microbiota drives early postnatal innate immune development[J]. Science, 2016, 351(6279): 1296-1302.
29 FER?EK I, LUGOVI?-MIHI? L, TAMBI?-ANDRA?EVI? A, et al. Features of the skin microbiota in common inflammatory skin diseases[J]. Life, 2021, 11(9): 962.
30 TA?EB A. Skin barrier in the neonate[J]. Pediatr Dermatol, 2018, 35(Suppl 1): s5-s9.
31 NISHIJIMA K, YONEDA M, HIRAI T, et al. Biology of the vernix caseosa: a review[J]. J Obstet Gynaecol Res, 2019, 45(11): 2145-2149.
32 MESFIN S, AFEWORK M, BIKILA D, et al. Distribution of vernix caseosa and associated factors among newborns delivered at Adama Comprehensive Specialized Hospital Medical College, Ethiopia, in 2022: cross-sectional study[J]. Clin Cosmet Investig Dermatol, 2022, 15: 2903-2914.
33 GRICE E A, KONG H H, CONLAN S, et al. Topographical and temporal diversity of the human skin microbiome[J]. Science, 2009, 324(5931): 1190-1192.
34 KONG H H. Skin microbiome: genomics-based insights into the diversity and role of skin microbes[J]. Trends Mol Med, 2011, 17(6): 320-328.
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