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The Role of the Microbiome in the Developmental Origins of Health and Disease Leah T

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The Role of the Microbiome in the Developmental Origins of Health and Disease Leah T The Role of the Microbiome inLeah T. Stiemsma,the PhD,Developmental Karin B. Michels, ScD, PhD Origins of Health and Disease abstract Although the prominent role of the microbiome in human health has been established, the early-life microbiome is now being recognized as a major influence on long-term human health and development.‍ Variations in the composition and functional potential of the early-life microbiome are the result of lifestyle factors, such as mode of birth, breastfeeding, diet, and antibiotic usage.‍ In addition, variations in the composition of the early-life NIH microbiome have been associated with specific disease outcomes, such as asthma, obesity, and neurodevelopmental disorders.‍ This points toward Department of Epidemiology, Fielding School of Public this bacterial consortium as a mediator between early lifestyle factors and Health, University of California, Los Angeles, Los Angeles, California health and disease.‍ In addition, variations in the microbial intrauterine environment may predispose neonates to specific health outcomes later in Dr Stiemsma conceptualized and outlined the review, conducted the literature search, drafted life.‍ A role of the microbiome in the Developmental Origins of Health and the initial manuscript, and reviewed and revised Disease is supported in this collective research.‍ Highlighting the early-life the manuscript; Dr Michels supervised the project critical window of susceptibility associated with microbiome development, and critically reviewed and edited the manuscript; and all authors approved the final manuscript as we discuss infant microbial colonization, beginning with the maternal- submitted and agreed to be accountable for all to-fetal exchange of microbes in utero and up through the influence of aspects of the work. breastfeeding in the first year of life.‍ In addition, we review the available DOI: https:// doi. org/ 10. 1542/ peds. 2017- 2437 disease-specific evidence pointing toward the microbiome as a mechanistic Accepted for publication Nov 29, 2017 mediator in the Developmental Origins of Health and Disease.‍ Address correspondence to Karin B. Michels, ScD, PhD, Department of Epidemiology, Fielding School of Public Health, University of California, Los Angeles, During the past decade, the research surrounding the maturation 650 Charles E. Young Dr S, Los Angeles, CA 90095. E-mail: [email protected] microbiome has emerged as a1 major of the early-life microbiome and how contributor to human health.‍ It has transient variations in this bacterial PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, been suggested in current studies consortium can have long-term 1098-4275). that the early-life microbiome is a consequences for human health.‍ Copyright © 2018 by the American Academy of Pediatrics crucial factor for proper immune 2, 3 THE DOHAD: WHERE DOES THE development and long-term health.‍ MICROBIOME FIT? FINANCIAL DISCLOSURE: The authors have Transient microbial dysbiosis indicated they have no financial relationships during this time period has been relevant to this article to disclose. FUNDING: Dr Stiemsma is supported by T32 training associated with the development– of The developmental origins hypothesis immune-mediated, metabolic, and proposes variations in fetal and infant grant 5T32CA009142-37 from the National Cancer 4 7 Institute (NCI), National Institutes of Health (NIH). neurodevelopmental disorders.‍ programming through environmental Funded by the National Institues of Health (NIH). In addition, increasing evidence has exposures during a critical window 9 POTENTIAL CONFLICT OF INTEREST: The authors been used to support a vital role of early life.‍ Termed10, 11originally as the have indicated they have no potential conflicts of of the maternal and intrauterine Barker hypothesis, in which the interest to disclose. microbiomes 8in childhood health and association between fetal malnutrition development.‍ Collectively, these and hypertension later in life was a To cite: Stiemsma LT and Michels KB. The Role findings have been used to support focus, this theory has since expanded of the Microbiome in the Developmental Origins the microbiome as a key participant to account for many types of early- of Health and Disease. Pediatrics. 2018;141(4): in the Developmental Origins of life exposures and birth outcomes e20172437 Health and Disease (DOHaD).‍ In this associated with long-term health and review, we will discuss the current development.‍ For example, high birth Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 141, number 4, April 2018:e20172437 STATE-OF-THE-ART REVIEW ARTICLE weight is associated with an increase12, 13 in breast and colon cancer risk, and the underlying mechanism of this association may be related to intrauterine exposure9 to high levels of growth hormones.‍ Early-life infections and microbial exposures were not originally associated with DOHaD but were proposed as significant environmental influences on infant immune development in the hygiene14 hypothesis of allergic disease.‍ With the advancement of human FIGURE 1 microbiome research, a modern The infant microbiome is most vulnerable to environmental influences in early life. Maternal to fetal microbial transfer, mode of birth, antibiotics, and diet can alter the colonization and maturation of extension of the hygiene hypothesis the early-life microbiome. These lifestyle-induced variations in microbiome composition and function has since been proposed, known15 as can have prolonged influences on human health and may lead to the development of disease later the microflora hypothesis.‍ In the in life. microflora hypothesis, it is suggested that early-life environmental exposures alter the development15 of the human microbiome.‍ the developmental origins field molecular techniques in the amniotic Shifts in the composition of the (Fig 1).‍ fluid and19, placentas 20 of healthy microbiome are thought to bias EARLY-LIFE DEVELOPMENT OF THE infants, suggesting a maternal- maturation of the immune system MICROBIOME to-fetal exchange of microbes.‍ In addition, through comparisons toward a hypersensitive and/or15 hyperinflammatory state.‍ For of the amniotic, placental, and example, the innate and adaptive The human microbiota is a composite meconium21 microbiotas, Collado et al report that the meconium branches of the immune system are organism, composed of 10 trillion to ∼ both highly involved in promoting 100 trillion microbial cells (bacteria, microbiota of infants delivered via an inflammatory response.‍ However, archaea, and microbial eukaryotes) cesarean delivery shares 55% of – 16, 17 exposure to microbes typically and viruses.‍ To highlight the its bacterial taxa with the placenta evokes a T-helper 1 mediated impressive functional potential and amniotic fluid microbiotas.‍ The of the microbiota, the genomic prenatal maternal microbiome may response, which suppresses ∼ the T-helper 2 activity often catalog of this super organism, the also modulate the Escherichiainfant immune coli microbiome, is composed of 3.‍3 system.‍ For example, gestation-only associated with immune-mediated3 “ 16 ” million nonredundant genes.‍ colonization with and hypersensitivity reactions.‍ “ ” Discussion of the mechanisms Although the terms microbiota HA107 was reported to modify the regulating the interface between the and microbiome are descriptive intestinal mucosal innate immune immune system and the microbiota of the microbial composition and system and22 transcriptome of the genomic catalog, respectively, they offspring.‍ is beyond the scope of this3 review; please see Tamburini et al for a are used interchangeably within this recent in-depth discussion on this research field.‍ The following sections In humans, variations in the placental topic.‍ are devoted to delineating the initial microbiome composition have colonization and establishment of been associated with maternal Analogous to DOHaD, an early-life the human bacterial microbiota in pregnancy-related (stress and critical window of development infancy, from conception through the gestational diabetes)– and neonatal Maternal-to-Fetalfirst year of life.‍ Microbial Transfer has also been proposed for the health outcomes7, 23(birth25 weight, microbiome.‍ Transient microbial preterm birth).‍ The placental dysbiosis (unhealthy microbial state) microbiome of infants born preterm during this time frame has been Until recently, the intrauterine was also reported to differ in associated with long-term immune2 environment18 was perceived as composition26 according to gestational and metabolic health issues, sterile.‍ However, nonpathogenic weight gain, suggesting that this meriting its exploration within bacteria have since been detected by bacterial consortium may mediate Downloaded from www.aappublications.org/news by guest on September 28, 2021 2 STIEMSMA and MICHELS fetal development depending on the meconium, etc) of cesarean delivered the first study aimed at recolonizing ’ health status of the mother.‍ infants areStaphylococcus initially populated with infants delivered via cesarean bacteria residing on the mother s delivery with vaginal bacteria.‍ After Isolation of bacteria from the skin (eg, spp.‍), swabbing neonates with maternal placenta is often associated with whereas vaginally delivered infants vaginal fluids within 2 minutes of a pathophysiological state, which Prevotella Atopobium are populated with typical vaginal birth, the authors report partial threatens the health of the mother bacteria
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