Maternal and infant microbiome: next-generation indicators and targets for intergenerational health and nutrition care

Abstract

Microbes are commonly sensitive to shifts in the physiological and pathological state of their hosts, including mothers and babies. From this perspective, the microbiome may be a good indicator for diseases during pregnancy and has the potential to be used for perinatal health monitoring. This is embodied in the application of microbiome from multi body sites for auxiliary diagnosis, early prediction, prolonged monitoring, and retrospective diagnosis of pregnancy and infant complications, as well as nutrition management and health products developments of mothers and babies. Here we summarized the progress in these areas and explained that the microbiome of different body sites is sensitive to different diseases and their microbial biomarkers may overlap between each other, thus we need to make a diagnosis prudently for those diseases. Based on the microbiome variances and additional anthropometric and physical data, individualized responses of mothers and neonates to meals and probiotics/prebiotics were predictable, which is of importance for precise nutrition and probiotics/prebiotics managements and developments. Although a great deal of encouraging performance was manifested in previous studies, the efficacy could be further improved by combining multi-aspect data such as multi-omics and time series analysis in the future. This review reconceptualizes maternal and infant health from a microbiome perspective, and the knowledge in it may inspire the development of new options for the prevention and treatment of adverse pregnancy outcomes and bring a leap forward in perinatal health care.

Keywords

newborn / microbiome / disease detection / pregnancy management / health care products

References

[1] Abrahamsson TR, Jakobsson HE, Andersson AF et al. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy 2014;44:842–850.

[2] ACOG. Diagnosis and management of preeclampsia and eclampsia. Int J Gynecol Obstet 2002;99:159–167.

[3] ADA. Classification and diagnosis of diabetes: standards of medical care in diabetes-2018. Diabetes Care 2018;41:S13–S27.

[4] Agarwal M, Boulvain M, Coetzee E et al. Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: a World Health Organization Guideline. Diabetes Res Clin Pract 2014;103:341–363.

[5] Alayande KA, Aiyegoro OA, Nengwekhulu TM et al. Integrated genome-based probiotic relevance and safety evaluation of Lactobacillus reuteri PNW1. PLoS One 2020;15:e0235873.

[6] Anhê FF, Roy D, Pilon G et al. A polyphenol-rich cranberry extract protects from diet-induced obesity, insulin resistance and intestinal inflammation in association with increased Akkermansia spp. population in the gut microbiota of mice. Gut 2015;64:872–883.

[7] Aragón IM, Herrera-Imbroda B, Queipo-Ortuño MI et al. The urinary tract microbiome in health and disease. Eur Urol focus 2018;4:128–138.

[8] Azad MB, Konya T, Maughan H et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. Can Med Assoc J 2013;185:385–394.

[9] Bafeta A, Koh M, Riveros C et al. Harms reporting in randomized controlled trials of interventions aimed at modifying microbiota: a systematic review. Ann Intern Med 2018;169:240–247.

[10] Bashiardes S, Zilberman-Schapira G, Elinav E. Use of meta-transcriptomics in microbiome research. Bioinf Biol Insights 2016;10:19–25.

[11] Becerra-Mojica CH, Parra-Saavedra MA, Diaz-Martinez LA et al. Cohort profile: Colombian Cohort for the Early Prediction of Preterm Birth (COLPRET): early prediction of preterm birth based on personal medical history, clinical characteristics, vaginal microbiome, biophysical characteristics of the cervix and maternal serum biochemical markers. BMJ Open 2022;12:e060556.

[12] Beckers KF, Sones JL. Maternal microbiome and the hypertensive disorder of pregnancy, preeclampsia. Am J Physiol Heart Circ Physiol 2020;318:H1–H10.

[13] Bereswill S, Muñoz M, Fischer A et al. Anti-inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation. PLoS One 2010;5:e15099.

[14] Berry SE, Valdes AM, Drew DA et al. Human postprandial responses to food and potential for precision nutrition. Nat Med 2020;26:964–973.

[15] Besselink MG, van Santvoort HC, Buskens E et al.; Dutch Acute Pancreatitis Study Group. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 2008;371:651–659.

[16] Blanton LV, Charbonneau MR, Salih T et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 2016;351:add3311–add3317.

[17] Blostein F, Bhaumik D, Davis E et al. Evaluating the ecological hypothesis: early life salivary microbiome assembly predicts dental caries in a longitudinal case-control study. Microbiome 2022;10:240.

[18] Bosheva M, Tokodi I, Krasnow A et al. Infant formula with a specific blend of five human milk oligosaccharides drives the gut microbiota development and improves gut maturation markers: a randomized controlled trial. Front Nutr 2022;9:1–14.

[19] Brodin P. Immune-microbe interactions early in life: a determinant of health and disease long term. Science 2022;376:945–950.

[20] Buffington SA, Di Prisco GV, Auchtung TA et al. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 2016;165:1762–1775.

[21] Buffington SA, Dooling SW, Sgritta M et al. Dissecting the contribution of host genetics and the microbiome in complex behaviors. Cell 2021;184:1740–1756.e1716.

[22] Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol 2015;11:577–591.

[23] Carpenter D, Dhar S, Mitchell LM et al. Obesity, starch digestion and amylase: association between copy number variants at human salivary (AMY1) and pancreatic (AMY2) amylase genes. Hum Mol Genet 2015;24:3472–3480.

[24] Chan D, Bennett PR, Lee YS et al. Microbial-driven preterm labour involves crosstalk between the innate and adaptive immune response. Nat Commun 2022;13:975.

[25] Chang Y, Chen Y, Zhou Q et al. Short-chain fatty acids accompanying changes in the gut microbiome contribute to the development of hypertension in patients with preeclampsia. Clin Sci (Colch) 2020;134:289–302.

[26] Chen Y, Li Z, Tye KD et al. Probiotic supplementation during human pregnancy affects the gut microbiota and immune status. Front Cell Infect Microbiol 2019;9:1–12.

[27] Chen W, Wei K, He X et al. Identification of uterine microbiota in infertile women receiving in vitro fertilization with and without chronic endometritis. Front Cell Dev Biol 2021;9:1–11.

[28] Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet 2012;13:260–270.

[29] Clarke TC, Black LI, Stussman BJ et al. Trends in the use of complementary health approaches among adults: United States, 2002-2012. Nat Health Stat Rep 2015;79:1–16.

[30] Connolly N, Anixt J, Manning P et al. Maternal metabolic risk factors for autism spectrum disorder-an analysis of electronic medical records and linked birth data. Autism Res 2016;9:829–837.

[31] Craig SJC, Blankenberg D, Parodi ACL et al. Child weight gain trajectories linked to oral microbiota composition. Sci Rep 2018;8:14030.

[32] Crovesy L, Ostrowski M, Ferreira D et al. Effect of Lactobacillus on body weight and body fat in overweight subjects: a systematic review of randomized controlled clinical trials. Int J Obesity 2017;41:1607–1614.

[33] Crusell MKW, Hansen TH, Nielsen T et al. Gestational diabetes is associated with change in the gut microbiota composition in third trimester of pregnancy and postpartum. Microbiome 2018;6:89.

[34] Damm P, Mathiesen ER. Diabetes: therapy for gestational diabetes mellitus—time for a change? Nat Rev Endocrinol 2015;11:327–328.

[35] David LA, Maurice CF, Carmody RN et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014;505:559–563.

[36] De Filippo C, Cavalieri D, Di Paola M et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107:14691–14696.

[37] DiGiulio DB, Romero R, Amogan HP et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One 2008;3:e3056.

[38] Draper K, Ley C, Parsonnet J. Probiotic guidelines and physician practice: a cross-sectional survey and overview of the literature. Benef Microbes 2017;8:507–519.

[39] Dunstan DW, Kingwell BA, Larsen R et al. Breaking up prolonged sitting reduces postprandial glucose and insulin responses. Diabetes Care 2012;35:976–983.

[40] Fan X, Alekseyenko AV, Wu J et al. Human oral microbiome and prospective risk for pancreatic cancer: a population-based nested case-control study. Gut 2018;67:120–127.

[41] Feng L, Raman AS, Hibberd MC et al. Identifying determinants of bacterial fitness in a model of human gut microbial succession. Proc Natl Acad Sci USA 2020;117:2622–2633.

[42] Ferretti P, Pasolli E, Tett A et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 2018;24:133–145.e135.

[43] Fettweis JM, Serrano MG, Brooks JP et al. The vaginal microbiome and preterm birth. Nat Med 2019;25:1012–1021.

[44] Flaviani F, Hezelgrave NL, Kanno T et al. Cervicovaginal microbiota and metabolome predict preterm birth risk in an ethnically diverse cohort. JCI Insight 2021;6:e149257.

[45] Fonseca W, Malinczak CA, Fujimura K et al. Maternal gut microbiome regulates immunity to RSV infection in offspring. J Exp Med 2021;218:e20210235.

[46] Gardella C, Riley DE, Hitti J et al. Identification and sequencing of bacterial rDNAs in culture-negative amniotic fluid from women in premature labor. Am J Perinatol 2004;21:319–323.

[47] Garrido D, Ruiz-Moyano S, Lemay DG et al. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci Rep 2015;5:13517.

[48] Gibbs EM, Stock JL, McCoid SC et al. Glycemic improvement in diabetic db/db mice by overexpression of the human insulin-regulatable glucose transporter (GLUT4). J Clin Invest 1995;95:1512–1518.

[49] Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995;125:1401–1412.

[50] Godfrey KM, Barton SJ, El-Heis S et al.; NiPPeR Study Group. Myo-Inositol, probiotics, and micronutrient supplementation from preconception for glycemia in pregnancy: NiPPeR International Multicenter Double-Blind Randomized Controlled Trial. Diabetes Care 2021;44:1091–1099.

[51] Gomez-Arango LF, Barrett HL, McIntyre HD et al. Increased systolic and diastolic blood pressure is associated with altered gut microbiota composition and butyrate production in early pregnancy. Hypertension 2016;68:974–981.

[52] Grześkowiak L, Collado MC, Mangani C et al. Distinct gut microbiota in southeastern African and northern European infants. J Pediatr Gastroenterol Nutr 2012;54:812–816.

[53] Gupta S, Ross TD, Gomez MM et al. Investigating the dynamics of microbial consortia in spatially structured environments. Nat Commun 2020;11:2418.

[54] Guyonnet D, Schlumberger A, Mhamdi L et al. Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study. Br J Nutr 2009;102:1654–1662.

[55] Hanson MA, Gluckman PD. Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev 2014;94:1027–1076.

[56] Hawrylyshyn PA, Bernstein P, Papsin FR. Risk factors associated with infection following cesarean section. Am J Obstet Gynecol 1981;139:294–298.

[57] Heavey MK, Durmusoglu D, Crook N et al. Discovery and delivery strategies for engineered live biotherapeutic products. Trends Biotechnol 2022;40:354–369.

[58] Henrick BM, Rodriguez L, Lakshmikanth T et al. Bifidobacteriamediated immune system imprinting early in life. Cell 2021;184:3884–3898.e11.

[59] Hillier SL, Martius J, Krohn M et al. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med 1988;319:972–978.

[60] Hillier SL, Witkin SS, Krohn MA et al. The relationship of amniotic fluid cytokines and preterm delivery, amniotic fluid infection, histologic chorioamnionitis, and chorioamnion infection. Obstet Gynecol 1993;81:941–948.

[61] Himsworth HP. Dietetic factors influencing the glucose tolerance and the activity of insulin. J Physiol 1934;81:29–48.

[62] Hoffman DJ, Powell TL, Barrett ES et al. Developmental origins of metabolic diseases. Physiol Rev 2021;101:739–795.

[63] Honeycutt TC, El Khashab M, Wardrop RM et al. Probiotic administration and the incidence of nosocomial infection in pediatric intensive care: a randomized placebo-controlled trial. Pediatr Crit Care Med 2007;8:452–458.

[64] Huang L, Cai M, Li L et al. Gut microbiota changes in preeclampsia, abnormal placental growth and healthy pregnant women. BMC Microbiol 2021;21:265.

[65] Huang L, Pan G, Feng Y et al. Microbial network signatures of early colonizers in infants with eczema. iMeta 2023;2:1–16.

[66] Huda MN, Ahmad SM, Alam MJ et al. Bifidobacterium abundance in early infancy and vaccine response at 2 years of age. Pediatrics 2019;143:e20181489.

[67] IADPSG. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 2010;33:676–682.

[68] Jin J, Gao L, Zou X et al. Gut dysbiosis promotes preeclampsia by regulating macrophages and trophoblasts. Circul Res 2022;131:492–506.

[69] Jo H, Eckel SP, Chen J-C et al. Gestational diabetes mellitus, prenatal air pollution exposure, and autism spectrum disorder. Environ Int 2019;133:105110.

[70] Johns EC, Denison FC, Norman JE et al. Gestational diabetes mellitus: mechanisms, treatment, and complications. Trends Endocrinol Metab 2018;29:743–754.

[71] Johnson BR, Hymes J, Sanozky-Dawes R et al. Conserved S-layer-associated proteins revealed by exoproteomic survey of S-layer-forming Lactobacilli. Appl Environ Microbiol 2016;82:134–145.

[72] Juan J, Yang H. Prevalence, prevention, and lifestyle intervention of gestational diabetes mellitus in China. Int J Env Res Public Health 2020;17:1–14.

[73] Kapse NG, Engineer AS, Gowdaman V et al. Functional annotation of the genome unravels probiotic potential of Bacillus coagulans HS243. Genomics 2019;111:921–929.

[74] Kindschuh WF, Baldini F, Liu MC et al. Preterm birth is associated with xenobiotics and predicted by the vaginal metabolome. Nat Microbiol 2023;8:246–259.

[75] Koren O, Goodrich JK, Cullender TC et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012;150:470–480.

[76] Krakowiak P, Walker CK, Bremer AA et al. Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics 2012;129:e1121–e1128.

[77] Kyburz A, Fallegger A, Zhang X et al. Transmaternal Helicobacter pylori exposure reduces allergic airway inflammation in offspring through regulatory T cells. J Allergy Clin Immunol 2019;143:1496–1512.e1411.

[78] Lende M, Rijhsinghani A. Gestational diabetes: overview with emphasis on medical management. Int J Env Res Public Health 2020;17:1–12.

[79] Leung H, Long X, Ni Y et al. Risk assessment with gut microbiome and metabolite markers in NAFLD development. Sci Transl Med 2022;14:eabk0855.

[80] Li N, Yang J, Zhang J et al. Correlation of gut microbiome between ASD children and mothers and potential biomarkers for risk assessment. Genomics Proteomics Bioinformatics 2019;17:26–38.

[81] Li N, An H, Li Z et al. Preconception blood pressure and risk of gestational hypertension and preeclampsia: a large cohort study in China. Hypertens Res 2020;43:956–962.

[82] Li X, Zheng J, Ma X et al. The oral microbiome of pregnant women facilitates gestational diabetes discrimination. J Genet Genomics 2021;48:32–39.

[83] Li X, Zhang B, Zheng J et al. Clinical biochemical indicators and intestinal microbiota testing reveal the influence of reproductive age extending from the mother to the offspring. Microbiol Spectr 2022;10:e01076–e01022.

[84] Liang X, Miao Z, Lu S et al. Integration of multiomics with precision nutrition for gestational diabetes: study protocol for the Westlake Precision Birth Cohort. iMeta 2023;2:1–12.

[85] Lim AI, McFadden T, Link VM et al. Prenatal maternal infection promotes tissue-specific immunity and inflammation in offspring. Science 2021;373:1–14.

[86] Liu AT, Chen S, Jena PK et al. Probiotics improve gastrointestinal function and life quality in pregnancy. Nutrients 2021;13:3931.

[87] Llorens-Rico V, Simcock JA, Huys GRB et al. Single-cell approaches in human microbiome research. Cell 2022;185:2725–2738.

[88] Lopez-Moreno A, Aguilera M. Probiotics dietary supplementation for modulating endocrine and fertility microbiota dysbiosis. Nutrients 2020;12:757.

[89] Lundgren SN, Madan JC, Emond JA et al. Maternal diet during pregnancy is related with the infant stool microbiome in a delivery mode-dependent manner. Microbiome 2018;6:109.

[90] Mackeen AD, Packard RE, Ota E et al. Antibiotic regimens for postpartum endometritis. The Cochrane Database Syst Rev 2015;2015:1–99.

[91] Macklaim JM, Gloor GB, Anukam KC et al. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci USA 2011;108:4688–4695.

[92] Mariat D, Firmesse O, Levenez F et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 2009;9:123.

[93] Martín-Peláez S, Cano-Ibáñez N, Pinto-Gallardo M et al. The impact of probiotics, prebiotics, and synbiotics during pregnancy or lactation on the intestinal microbiota of children born by cesarean section: a systematic review. Nutrients 2022;14:341.

[94] Matusheski NV, Caffrey A, Christensen L et al. Diets, nutrients, genes and the microbiome: recent advances in personalised nutrition. Br J Nutr 2021;126:1489–1497.

[95] McIntyre HD, Catalano P, Zhang C et al. Gestational diabetes mellitus. Nat Rev Dis Primers 2019;5:47.

[96] Neyrinck AM, Van Hée VF, Bindels LB et al. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: potential implication of the gut microbiota. Br J Nutr 2013;109:802–809.

[97] Olabi B, Bhopal R. Diagnosis of diabetes using the oral glucose tolerance test. Bmj 2009;339:b4354.

[98] Onderdonk AB, Delaney ML, Fichorova RN. The human microbiome during bacterial vaginosis. Clin Microbiol Rev 2016;29:223–238.

[99] Oozeer R, van Limpt K, Ludwig T et al. Intestinal microbiology in early life: specific prebiotics can have similar functionalities as humanmilk oligosaccharides. Am J Clin Nutr 2013;98:561S561s–561S571S.

[100] Panigrahi P, Parida S, Nanda NC et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature 2017;548:407–412.

[101] Park S, Oh D, Heo H et al. Prediction of preterm birth based on machine learning using bacterial risk score in cervicovaginal fluid. Am J Reprod Immunol 2021;86:e13435.

[102] Park S, Moon J, Kang N et al. Predicting preterm birth through vaginal microbiota, cervical length, and WBC using a machine learning model. Front Microbiol 2022;13:1–11.

[103] Plows JF, Stanley JL, Baker PN et al. The Pathophysiology of Gestational Diabetes Mellitus. Int J Mol Sci 2018;19:3342.

[104] Pinto Y, Frishman S, Turjeman S et al. Gestational diabetes is driven by microbiota-induced inflammation months before diagnosis. Gut 2023;0:1–11.

[105] Purushe J, Fouts DE, Morrison M et al. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 2010;60:721–729.

[106] Quince C, Walker AW, Simpson JT et al. Shotgun metagenomics, from sampling to analysis. Nat Biotechnol 2017;35:833–844.

[107] Romero R, Sirtori M, Oyarzun E et al. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol 1989;161:817–824.

[108] Rondanelli M, Faliva MA, Perna S et al. Using probiotics in clinical practice: where are we now? A review of existing meta-analyses. Gut Microbes 2017;8:521–543.

[109] Samara J, Moossavi S, Alshaikh B et al. Supplementation with a probiotic mixture accelerates gut microbiome maturation and reduces intestinal inflammation in extremely preterm infants. Cell Host Microbe 2022;30:696–711.e5.

[110] Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 1977;31:107–133.

[111] Scholtens PA, Goossens DAM, Staiano A. Stool characteristics of infants receiving short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides: a review. World J Gastroenterol 2014;20:13446–13452.

[112] Schwarzer M, Makki K, Storelli G et al. Lactobacillus plantarum strain maintains growth of infant mice during chronic under-nutrition. Science 2016;351:854–857.

[113] Sgritta M, Dooling SW, Buffington SA et al. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 2019;101:246–259.e246.

[114] Shao Y, Forster SC, Tsaliki E et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature 2019;574:117–121.

[115] Sibai BM. Diagnosis and management of gestational hypertension and preeclampsia. Obstet Gynecol 2003;102:181–192.

[116] Smith MI, Yatsunenko T, Manary MJ et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013;339:548–554.

[117] Stewart CJ, Ajami NJ, O’Brien JL et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 2018;562:583–588.

[118] Subramanian S, Huq S, Yatsunenko T et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 2014;510:417–421.

[119] Sullivan EL, Nousen EK, Chamlou KA. Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol Behav 2014;123:236–242.

[120] Sun J, Buys NJ. Glucose- and glycaemic factor-lowering effects of probiotics on diabetes: a meta-analysis of randomised placebo- controlled trials. Br J Nutr 2016;115:1167–1177.

[121] Sun Z, Pan XF, Li X et al. The gut microbiome dynamically associates with host glucose metabolism throughout pregnancy: longitudinal findings from a matched case-control study of gestational diabetes mellitus. Adv Sci 2023;22:e2205289.

[122] Tang B, Tang L, Li S et al. Gut microbiota alters host bile acid metabolism to contribute to intrahepatic cholestasis of pregnancy. Nat Commun 2023;14:1305.

[123] Teng F, Yang F, Huang S et al. Prediction of early childhood caries via spatial-temporal variations of oral microbiota. Cell Host Microbe 2015;18:296–306.

[124] Victora CG, de Onis M, Hallal PC et al. Worldwide timing of growth faltering: revisiting implications for interventions. Pediatrics 2010;125:e473–e480.

[125] Vogel G. Deaths prompt a review of experimental probiotic therapy. Science 2008;319:557–557.

[126] Wampach L, Heintz-Buschart A, Fritz JV et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat Commun 2018;9:5091.

[127] Wang J, Zheng J, Shi W et al. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut 2018;67:1614–1625.

[128] Wang S, Ryan CA, Boyaval P et al. Maternal vertical transmission affecting early-life microbiota development. Trends Microbiol 2020;28:28–45.

[129] Wang J, Li Z, Ma X et al. Translocation of vaginal microbiota is involved in impairment and protection of uterine health. Nat Commun 2021;12:4191.

[130] Wang J, Xiao L, Xiao B et al. Maternal and neonatal viromes indicate the risk of offspring’s gastrointestinal tract exposure to pathogenic viruses of vaginal origin during delivery. mLife 2022;1:303–310.

[131] Weinert LS. International Association of Diabetes and Pregnancy Study Groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy: comment to the International Association of Diabetes and Pregnancy Study Groups Consensus Panel. Diabetes Care 2010;33:e97–e97.

[132] Whiteside SA, Razvi H, Dave S et al. The microbiome of the urinary tract--a role beyond infection. Nat Rev Urol 2015;12:81–90.

[133] Wu H, Dong C, Xiao W et al. Associations between PM(2.5) exposure and infant growth: a mediation analysis of oral microbiota. Sci Total Environ 2022;823:153688.

[134] Xiao J, Fiscella KA, Gill SR. Oral microbiome: possible harbinger for children’s health. Int J Oral Sci 2020;12:12.

[135] Xiao L, Wang J, Zheng J et al. Deterministic transition of enterotypes shapes the infant gut microbiome at an early age. Genome Biol 2021;22:1–21.

[136] Yang Y, Le Ray I, Zhu J et al. Preeclampsia prevalence, risk factors, and pregnancy outcomes in Sweden and China. JAMA Netw Open 2021;4:e218401.

[137] Yao X, Zuo N, Guan W et al. Association of gut microbiota enterotypes with blood trace elements in women with infertility. Nutrients 2022;14:3195.

[138] Yassour M, Vatanen T, Siljander H et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci Transl Med 2016;8:1–12.

[139] Yoon BH, Romero R, Moon JB et al. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2001;185:1130–1136.

[140] Yu Y, Zhang B, Ji P et al. Changes to gut amino acid transporters and microbiome associated with increased E/I ratio in Chd8(+/−) mouse model of ASD-like behavior. Nat Commun 2022;13:1151.

[141] Zeevi D, Korem T, Zmora N et al. Personalized nutrition by prediction of glycemic responses. Cell 2015;163:1079–1094.

[142] Zhang Q, Wu Y, Fei X. Effect of probiotics on body weight and body-mass index: a systematic review and meta-analysis of randomized, controlled trials. Int J Food Sci Nutr 2015;67: 571–580.

[143] Zhang X, Zhai Q, Wang J et al. Variation of the vaginal microbiome during and after pregnancy in Chinese women. Genomics Proteomics Bioinformatics 2022;20:322–333.

[144] Zheng W, Xu Q, Huang W et al. Gestational diabetes mellitus is associated with reduced dynamics of gut microbiota during the first half of pregnancy. mSystems 2020a;5:e00109–e00120.

[145] Zheng W, Zhao W, Wu M et al. Microbiota-targeted maternal antibodies protect neonates from enteric infection. Nature 2020b;577:543–548.

[146] Zhu WW, Yang HX, Wei YM et al. Evaluation of the value of fasting plasma glucose in the first prenatal visit to diagnose gestational diabetes mellitus in china. Diabetes Care 2013;36:586–590.

[147] Zmora N, Zilberman-Schapira G, Suez J et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 2018;174:1388–1405.e1321.

RIGHTS & PERMISSIONS

2023 The Author(s) 2023. Published by Oxford University Press on behalf of Higher Education Press.