孕妇肠道、阴道菌群和新生儿胎粪、胎皮脂菌群的相关性研究

doi:10.3969/j.issn.1674-8115.2024.01.006

上海交通大学学报（医学版） ›› 2024, Vol. 44 ›› Issue (1): 50-63.doi: 10.3969/j.issn.1674-8115.2024.01.006

孕妇肠道、阴道菌群和新生儿胎粪、胎皮脂菌群的相关性研究

马锦倩¹^,²(), 范翩翩¹(), 郑涛¹^,³, 张琳³^,⁴, 陈远志¹, 申剑⁵, 欧阳凤秀¹^,²()

^1.上海交通大学医学院附属新华医院环境与儿童健康教育部和上海市重点实验室，上海 200092
^2.上海体育大学运动健康学院，上海 200438
^3.上海交通大学医学院附属新华医院妇产科，上海 200092
^4.上海交通大学医学院附属国际和平妇幼保健院产科，上海 200030
^5.上海交通大学系统生物医学研究院，系统生物医学教育部重点实验室，上海 200240

收稿日期:2023-06-09 接受日期:2023-12-05 出版日期:2024-01-28 发布日期:2024-02-28
通讯作者: 欧阳凤秀 E-mail:mjq18335988098@126.com;447259743@qq.com;ouyangfengxiu@xinhuamed.com.cn
作者简介:马锦倩（1999—），女，硕士生；电子信箱：mjq18335988098@126.com
范翩翩（1990—），女，博士生；电子信箱：447259743@qq.com第一联系人：（马锦倩、范翩翩并列第一作者）
基金资助:
国家重点研发计划重点专项(2017YFE0124700);国家自然科学基金(81961128023);上海交通大学医学院“双百人”项目(20152518)

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

MA Jinqian¹^,²(), FAN Pianpian¹(), ZHENG Tao¹^,³, ZHANG Lin³^,⁴, CHEN Yuanzhi¹, SHEN Jian⁵, OUYANG Fengxiu¹^,²()

^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

Received:2023-06-09 Accepted:2023-12-05 Online:2024-01-28 Published:2024-02-28
Contact: OUYANG Fengxiu E-mail:mjq18335988098@126.com;447259743@qq.com;ouyangfengxiu@xinhuamed.com.cn
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)

摘要/Abstract

摘要：

目的·分析母亲孕晚期肠道菌群、阴道菌群、新生儿胎粪及胎皮脂菌群的多样性及菌群构成，比较其异同及相关性。方法·前瞻性研究。招募2018年8月—11月于上海交通大学医学院附属新华医院分娩的11对母婴，采集母亲孕晚期粪便样本、阴道拭子及新生儿胎粪；招募2018年12月于上海交通大学医学院附属国际和平妇幼保健院分娩的14名新生儿，采集额部、腋窝、腹股沟部位的胎皮脂及胎粪样本。所有孕妇均为阴道自然分娩。采用16S rRNA基因V3~V4区测序进行微生物检测，分析11对母婴中母亲的肠道菌群、阴道菌群和新生儿的胎粪菌群，以及14名新生儿的胎皮脂菌群和胎粪菌群的多样性、菌群构成，分析异同及相关性。结果·母亲肠道菌群的操作分类单元（operational taxonomic unit，OTU）数、Ace指数、Chao1指数、Shannon指数均高于阴道菌群和新生儿胎粪菌群；新生儿3个部位胎皮脂菌群的Ace指数和Chao1指数均显著高于胎粪菌群（均P<0.01）。母亲肠道菌群、阴道菌群和新生儿胎粪菌群β多样性存在差异（P<0.01）；新生儿额部、腋窝和腹股沟3个部位胎皮脂菌群的β多样性相似，但与胎粪菌群存在差异（P<0.01）。在门水平上，母亲肠道菌群优势菌主要为厚壁菌门（Firmicutes，52.76%）和拟杆菌门（Bacteroidetes，41.67%），阴道菌群优势菌为厚壁菌门（74.36%）和放线菌门（Actinobacteria，21.25%），胎皮脂菌群的优势菌为厚壁菌门（84.22%）和变形菌门（Proteobacteria，8.80%），新生儿胎粪菌群在2个批次样本中优势菌均为变形菌门（分别占81.11%和88.72%）。在属水平上，母亲肠道菌群的优势菌为拟杆菌属（Bacteroides，35.42%）和栖粪杆菌属（Faecalibacterium，10.12%），阴道菌群的优势菌为乳杆菌属（Lactobacillus，69.10%）和双歧杆菌属（Bifidobacterium，11.30%），胎皮脂菌群的优势菌为乳杆菌属（79.81%）和假单胞菌属（Pseudomonas，3.23%），胎粪菌群的优势菌在2个批次样本中均为埃希菌属（Escherichia，分别占55.21%和31.18%）。结论·母亲孕晚期肠道菌群的α多样性高于阴道菌群和新生儿胎粪菌群，新生儿胎皮脂菌群α多样性高于胎粪菌群。厚壁菌门在母亲孕晚期肠道菌群、阴道菌群及新生儿胎皮脂菌群中均为优势菌，乳杆菌属在母亲阴道菌群及新生儿胎皮脂菌群中均为优势菌，胎粪菌群以变形菌门和埃希菌属较多。新生儿不同身体部位的胎皮脂菌群结构相似，但与胎粪菌群存在差异。

关键词: 母婴菌群的垂直传递, 肠道菌群, 阴道菌群, 胎粪菌群, 胎皮脂菌群, 新生儿

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.

Key words: vertical transmission of mother-infant microbiota, gut microbiota, vaginal microbiota, meconium microbiota, vernix caseosa microbiota, newborn

中图分类号:

马锦倩, 范翩翩, 郑涛, 张琳, 陈远志, 申剑, 欧阳凤秀. 孕妇肠道、阴道菌群和新生儿胎粪、胎皮脂菌群的相关性研究[J]. 上海交通大学学报（医学版）, 2024, 44(1): 50-63.

MA Jinqian, FAN Pianpian, ZHENG Tao, ZHANG Lin, CHEN Yuanzhi, SHEN Jian, OUYANG Fengxiu. 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.

图/表 11

表1 11对母婴的临床特征

Tab 1 Clinical characteristics of 11 pairs of mothers and newborns

Characteristic	Value	Characteristic	Value
Maternal characteristic (n=11)		Weight gain in mid to late pregnancy/kg	12.69±4.50
Age/year	29.00±4.03	Gestational diabetes mellitus/n(%)	1(9.1)
Education level/n(%)		GBS positive/n(%)	0(0)
High school or below	3(27.3)	Puerperal fever/n(%)	0(0)
College or above	8(72.7)	Infant characteristic (n=11)
Parity/n(%)		Infant gender/n(%)
0	8(72.7)	Girl	4(36.4)
≥1	3(27.3)	Boy	7(63.6)
Antibiotics use during child delivery/n(%)		Weight for gestational age/n(%)
No	8(72.7)	SGA	2(18.2)
Yes	3(27.3)	AGA	8(72.7)
Early pregnancy BMI/n(%)		LGA	1(9.1)
<18.5 kg·m^-2	0(0)	Entering NICU after birth/n(%)
18.5‒23.9 kg·m^-2	8(72.7)	Yes	1 (9.1)
24.0‒27.9 kg·m^-2	1(9.1)	No	10(90.9)
≥28 kg·m^-2	2(18.2)	Gestational age at birth/week	40.18±0.75
Pre-delivery BMI/n(%)		Length/cm	50.27±1.62
<18.5 kg·m^-2	0(0)	Birth weight/g	3 536.36±423.66
18.5‒23.9 kg·m^-2	0(0)	Head circumference/cm	34.55±1.21
24.0‒27.9 kg·m^-2	6(54.5)	Birth BMI/(kg·m^-2)	13.96±1.15
≥28 kg·m^-2	5(45.5)	Neonatal antibiotics use/n(%)	0(0)

表2 14名新生儿及其母亲的临床特征

Tab 2 Clinical characteristics of 14 newborns and their mothers

Characteristic	Value	Characteristic	Value
Maternal characteristic (n=14)		Weight gain in mid to late pregnancy/kg	11.09±9.63
Age/year	30.43±2.90	Gestational diabetes mellitus/n(%)	1(7.1)
Education level/n(%)		GBS positive/n(%)	0(0)
High school or below	3(21.4)	Puerperal fever/n(%)	0(0)
College or above	11(78.6)	Infant characteristic (n=14)
Parity/n(%)		Infant gender/n(%)
0	10(71.4)	Girl	7(50.0)
≥1	4(28.6)	Boy	7(50.0)
Antibiotics use during child delivery/n(%)		Weight for gestational age/n(%)
No	11(78.57)	SGA	0(0)
Yes	3(21.43)	AGA	10(71.4)
Early pregnancy BMI/n(%)		LGA	4(28.6)
<18.5 kg·m^-2	0(0)	Entering NICU after birth/n(%)
18.5‒23.9 kg·m^-2	11(78.6)	Yes	2(14.3)
24.0‒27.9 kg·m^-2	2(14.3)	No	12(85.7)
≥28 kg·m^-2	1(7.1)	Gestational age at birth/week	39.14±0.95
Pre-delivery BMI/n(%)		Length/cm	50.00±0.88
<18.5 kg·m^-2	0(0)	Birth weight/g	3 418.93±371.51
18.5‒23.9 kg·m^-2	2(14.3)	Birth BMI/(kg·m^-2)	13.66±1.26
24.0‒27.9 kg·m^-2	8(57.1)	Neonatal antibiotics use/n(%)	0(0)
≥28 kg·m^-2	4(28.6)	－	－

图1 不同样本OTU数量的Venn图Note： A. Maternal gut microbiota, and vaginal microbiota in late-pregnancy and neonatal meconium microbiota from the 11 pairs of mothers and newborns. B. Neonatal vernix caseosa (at forehead, axilla, and inguinal crease) and meconium microbiota from the 14 newborns.

Fig 1 Venn diagrams of the OTU numbers from different samples

图2 母亲孕晚期肠道菌群、阴道菌群和新生儿胎粪菌群Ace (A), Chao1 (B), Shannon (C)及Simpson (D)指数箱型图Note： M—maternal gut microbiota; V—maternal vaginal microbiota; N—neonatal meconium microbiota.

Fig 2 Box plots of Ace (A), Chao1 (B), Shannon (C), and Simpson (D) indices of maternal gut microbiota and vaginal microbiota in late-pregnancy and neonatal meconium microbiota

图3 新生儿胎皮脂菌群和胎粪菌群Ace (A), Chao1 (B), Shannon (C)及Simpson (D)指数箱型图Note： S1—neonatal vernix caseosa at forehead; S2—neonatal vernix caseosa at axilla; S3—neonatal vernix caseosa at inguinal crease; F—neonatal meconium.

Fig 3 Box plots of Ace (A), Chao1 (B), Shannon (C), and Simpson (D) indices of microbiota in neonatal vernix caseosa and meconium

图4 不同样本菌群β多样性PCoA分析Note： A. Maternal gut microbiota and vaginal microbiota in late-pregnancy and neonatal meconium microbiota from the 11 pairs of mothers and newborns. B. Neonatal vernix caseosa (at forehead, axilla, and inguinal crease) and meconium microbiota from the 14 newborns.

Fig 4 PCoA analysis of β diversity of the microbiota from different samples

图5 不同样本菌群门和属水平物种相对丰度柱形图Note： A/B. Maternal gut microbiota and vaginal microbiota in late-pregnancy and neonatal meconium microbiota from the 11 pairs of mothers and newborns at the levels of phylum (A) and genus (B). C/D. Neonatal vernix caseosa (at forehead, axilla, and inguinal crease) and meconium microbiota from the 14 newborns at the levels of phylum (C) and genus (D). M1?M11: maternal gut microbiota; V1?V11: maternal vaginal microbiota; N1?N11: neonatal meconium microbiota; S1-1?S1-8: neonatal vernix caseosa at forehead; S2-1?S2-10: neonatal vernix caseosa at axilla; S3-1?S3-10: neonatal vernix caseosa at inguinal crease; F-2, F-5, F-8, F-11?F-14: neonatal meconium.

Fig 5 Histogram of relative species abundance at the phylum and genus levels in different samples

图6 母亲孕晚期肠道菌群、阴道菌群、新生儿胎粪菌群门(A)和属(B)水平物种组成热图Note： Due to the potential significant differences in relative abundance of species, sample clustering was affected. After multiplying the relative abundance by 100, a log transformation with a base of 10 was performed [y=lg(100x)]. If the relative abundance of species in the sample was 0, it would be replaced with the log value of half of the minimum value (≠0) of species abundance in all samples.

Fig 6 Species composition heatmaps at the level of phylum (A) and genus (B) in the maternal gut microbiota and maternal vaginal microbiota in late-pregnancy and neonatal meconium microbiota

图7 母亲孕晚期肠道菌群、阴道菌群和新生儿胎粪菌群LEfSe分析进化分支图Note： Different colors in the figure represent different microbial communities. The yellow nodes represent microbial communities that do not play an important role in the 3 groups. The green nodes represent microbial communities that play an important role in the maternal gut microbiota. The blue nodes represent microbial communities that play an important role in the maternal vaginal microbiota. The red nodes represent microbial communities that play an important role in the neonatal meconium microbiota. From the inside out, each circle consists of species at the level of phylum, class, order, family, and genus.

Fig 7 LEfSe cladogram of analysis on the maternal gut microbiota, and vaginal microbiota in late-pregnancy and neonatal meconium microbiota

图8 新生儿胎皮脂菌群和胎粪菌群LEfSe分析进化分支图Note： The red nodes represent the microbial communities that play an important role in the neonatal vernix caseosa at forehead. The blue nodes represent the microbial communities that play an important role in the neonatal vernix caseosa at axilla. The green nodes represent the microbial communities that play an important role in the neonatal vernix caseosa at inguinal crease. The purple nodes represent the microbial communities that play an important role in neonatal meconium. From the inside out, each circle consists of species at the level of phylum, class, order, family, and genus.

Fig 8 LEfSe cladogram of analysis of the neonatal vernix caseosa microbiota and meconium microbiota

图9 不同样本菌群UPGMA分析Note： A. Maternal gut microbiota, and vaginal microbiota in late-pregnancy and neonatal meconium microbiota from the 11 pairs of mothers and newborns. B. Neonatal vernix caseosa (at forehead, axilla and inguinal crease) and meconium microbiota from the 14 newborns. M1?M11: maternal gut microbiota; V1?V11: maternal vaginal microbiota; N1?N11: neonatal meconium microbiota; S1-1?S1-8: neonatal vernix caseosa at forehead; S2-1?S2-10: neonatal vernix caseosa at axilla; S3-1?S3-10: neonatal vernix caseosa at inguinal crease; F-2, F-5, F-8, F-11?F-14: neonatal meconium.

Fig 9 UPGMA analysis of the microbiota from different samples

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孕妇肠道、阴道菌群和新生儿胎粪、胎皮脂菌群的相关性研究

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

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