The Developing Microbiota

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The Importance of the Microbiota


The Pregnancy Microbiome

Author(s): H. Neuman, O. Koren

In recent years, microbiome research has revealed multiple essential roles of the microorganisms residing within the human body in host metabolism, immunity, and overall health. Numerous physiological and pathological states, including obesity and the metabolic syndrome, have been correlated with microbial changes, termed dysbiosis. Our microbiomes change in response to our environment, diet, weight, hormones, and other factors. It is, therefore, not surprising that there are also significant changes in the microbiome during pregnancy when dramatic weight gain and metabolic and immunological changes occur. 

In this review, we summarize the known changes in microbial composition throughout pregnancy at a variety of body sites, including the gut, vagina, oral cavity, and placenta, and we describe several studies that have linked pregnancy complications with microbial changes. Unlike the case of certain disease states, such as obesity, where dysbiosis is considered to have negative effects, we believe that the microbial alterations observed during pregnancy are vital for a healthy pregnancy. 

While more research in this field is required to reveal specific mechanisms and pathways regulating these alterations, the microbial changes during pregnancy are likely coordinated with the immune, endocrine, and metabolic states.

Microbial Composition of the Initial Colonization of Newborns

Author(s): S. Rautava

Early-life interaction with indigenous intestinal microbes is a prerequisite for healthy immune and metabolic maturation. Human infants acquire their gut microbiota predominantly from the mother. A considerable inoculum of microbes is received by the neonate during vaginal delivery. 

Recent observations suggest that human gut colonization may be initiated prenatally by microbes in amniotic fluid, but the significance of this phenomenon remains unknown. After birth, neonatal gut colonization is guided by human milk factors, which selectively promote the growth of specific microbes, as well as by live microbes present in human milk. Aberrant gut colonization in early life has been associated with an increased risk of noncommunicable diseases in later life. 

Epidemiological and experimental studies suggest a causal relationship between early-life gut microbiota perturbations and disease risk. Perinatal antibiotic exposure, cesarean section delivery, postnatal antibiotic administration, and formula feeding, which may disrupt intestinal microecology, have been associated with disease development in later life. The modulation of gut microbiota in the perinatal period by pre- and probiotics, for example, may offer a means to reduce the risk of chronic diseases.

Bacterial Colonization of the Newborn Gut, Immune Development, and Prevention of Disease

Author(s): W. A. Walker

We now know that the fetus does not reside in a sterile intrauterine environment but is exposed to commensal bacteria from the maternal gut which cross the placenta and infiltrate the amniotic fluid. This exposure to colonizing bacteria continues at birth and during the first year of life, and it has a profound influence on lifelong health. Why is this important? 

Cross talk with colonizing bacteria in the developing neonatal intestine helps in the initial adaptation of the infant to extrauterine life, particularly in acquiring immune homeostasis, and provides protection against disease expression (e.g., allergy, autoimmune disease, and obesity) later in life. Colonizing intestinal bacteria are critical to the development of host defense during the neonatal period. 

Disrupted colonization (dysbiosis) due to cesarean section delivery, perinatal antibiotics, or premature delivery may adversely affect the development of host defense mechanisms in the gut and predispose to inflammation leading to increased susceptibility to disease later in life. Clinical evidence suggests that babies born by cesarean section have higher incidence rates of allergy, type 1 diabetes, and obesity. 

Infants given repeated antibiotic regimens are more likely to have asthma as adolescents. This observation helps to explain the disease paradigm shift in children from developed countries.

Gut-Brain Axis and Behavior

Author(s):  C. R. Martin, E. A. Mayer

In the last 5 years, interest in the interactions among the gut microbiome, brain, and behavior has exploded. Preclinical evidence supports a role of the gut microbiome in behavioral responses associated with pain, emotion, social interactions, and food intake. Limited, but growing, clinical evidence comes primarily from associations of gut microbial composition and function to behavioral and clinical features and brain structure and function. Converging evidence suggests that the brain and the gut microbiota are in bidirectional communication. 

Observed dysbiotic states in depression, chronic stress, and autism may reflect altered brain signaling to the gut, while altered gut microbial signaling to the brain may play a role in reinforcing brain alterations. On the other hand, primary dysbiotic states due to Western diets may signal to the brain, altering ingestive behavior. While studies performed in patients with depression and rodent models generated by fecal microbial transfer from such patients suggest causation, evidence for an influence of acute gut microbial alterations on human behavioral and clinical parameters is lacking. Only recently has an open-label microbial transfer therapy in children with autism tentatively validated the gut microbiota as a therapeutic target. The translational potential of preclinical findings remains unclear without further clinical investigation.

Dysbiosis in the Neonatal Period: Role of Cesarean Section

Author(s):  J. Neu

From epidemiological studies and studies done evaluating microbiomes in infants, there is a strong signal that the infants born by elective cesarean section (C-section) develop microbiota that differs from those babies born by vaginal delivery. 

Epidemiological studies show increased odds ratios for the development of immunological disorders such as type 1 diabetes, celiac disease, asthma, allergic diseases as well as metabolic diseases such as obesity in babies born by C-section. These are interesting associations, and if supported by additional studies that rigorously control for confounding factors, they will have major public health implications. 

Such studies represent major challenges because the confounding factors are numerous. The fact that provision of vaginal bacteria to C-sectiondelivered babies using a mouth swab that may actually transmit these bacteria to the infant is of interest and supports the concept that this can be done to alter the infant microbiota. However, significant caution needs to be taken, and alternative approaches that are safe as well as effective need to be considered; follow-up studies showing efficacy as well as safety need to be evaluated in the long term.

Early-Life Antibiotic Exposure, Gut Microbiota Development, and Predisposition to Obesity

Author(s):  M. B. Azad, S. Moossavi, A. Owora, S. Sepehri

Antibiotics are often prescribed inappropriately to infants and young children, with potentially adverse effects on the developing gut microbiota and related metabolic processes. We review evidence from 17 epidemiologic studies suggesting that antibiotic exposure during critical periods of early development may influence weight gain and the development of obesity. 

Complementary research in both humans and rodents indicates that gut microbiota play a key role in this process, although further research is needed to confirm and characterize the causal mechanisms involved. Obesity is a complex and multifactorial condition; thus, a multipronged prevention strategy will be required to curb the current obesity epidemic. Evidence to date suggests this strategy should include the judicious use of antibiotics, especially in early life when the developing gut microbiota is particularly susceptible to perturbations with long-lasting implications for metabolic programming and obesity risk.

Microbiota and Necrotizing Enterocolitis

Author(s):  S. Patole

Necrotizing enterocolitis (NEC) is an acquired gastrointestinal inflammatory condition with significant mortality and morbidity in preterm very low birth weight infants. The interplay between toll-like receptors, bacterial endotoxins, developmentally regulated excessive proinflammatory responses of the immature innate immune system, hypoxia, ischemia, reperfusion, free radicals, and the presence of substrates and bacterial endotoxins is thought to play an important role in the pathogenesis of NEC. The association (cause?) of various microbes (bacteria, viruses, and fungi) with NEC has intrigued researchers for many years. 

Availability of newer molecular methods (e.g., 16S ribosomal RNA gene-specific primers/pyrosequencing of fecal DNA) is expected to improve our understanding of the role of gut microbiota in the pathogenesis of NEC. Recent studies employing such methods to assess fecal microbiota are reviewed. Current evidence suggests that dysbiosis of the gut microbiota precedes the development of NEC in preterm infants. 

Further research is required to understand the significance of changes in the gut microbiome over the early postnatal period including the relative abundance of Gammaproteobacteria and the paucity of strict anaerobic bacteria that precedes NEC in preterm infants. Assessing the reproducibility of previous findings in large prospective studies with standardized methodology (e.g. sample processing, PCR primer, and DNA extraction) is important.

Microbiota and Obesity

Author(s):  E. Isolauri

Obesity is globally the most prevalent nutritional disorder. Multifaceted therapeutic approaches are called for to halt the cascade from neonatal adiposity/high birth weight to childhood excessive weight gain/adult obesity with comorbidities. Recent experimental and clinical data provide one new target for interventions aiming to close this vicious circle: the microbiota. 

An aberrant gut microbiota, dysbiosis, induces immune and metabolic disturbances both locally and, consequent upon impaired gut barrier function, also systemic low-grade inflammation, which is causally linked to insulin resistance. The gut microecology could thus fill the gap between energy intake and expenditure by processing nutrients and regulating their access to and storage in the body, producing chemicals of hormonal nature and controlling the secretion of proinflammatory mediators locally and systemically.

Conversely, being highly sensitive to environmental impacts, particularly to early feeding, the compositional development of the gut microbiota may prove the target of choice in efforts to reduce the risk of obesity. It has been demonstrated that a lower number of bifidobacteria precedes the development of obesity, and a dearth of butyrate-producing bacteria and an overall richness of bacteria increase the risk of metabolic disease; moreover, recognition that practices known to disrupt the early gut microbiota, e.g., cesarean section delivery and antibiotic exposure, contribute to obesity, encourages to pursue this line of research.

Diet and Gut Microbiota in Health and Disease

Author(s):  T. David Shen

Gut microbiota plays an important role in host health maintenance and disease pathogenesis. The development of a stable and diverse gut microbiota is essential to various host physiologic functions such as immunoregulation, pathogen prevention, energy harvest, and metabolism. At the same time, a dysbiotic gut microbiota associated with disease is altered in structure and function, and often characterized by a decrease in species richness and proliferation of pathogenic bacterial taxa. 

As a shared substrate between the host and the gut microbiota, diet significantly impacts the health and disease states of the host both directly and through gut microbial metabolite production. This is demonstrated in the examples of short-chain fatty acid and trimethylamine production via bacterial metabolism of dietary complex carbohydrates and choline, respectively. In disorders related to mucosal immune dysregulation such as inflammatory bowel disease, the dysbiotic gut microbiota and diet contribute to its pathogenesis. 

Reversal of dysbiosis through fecal microbiota transplantation and dietary interventions may thus represent important strategies to modify the gut microbiota and its metabolite production for health maintenance as well as disease prevention and management.

Differential Establishment of Bifidobacteria in the Breastfed Infant Gut

Author(s):  Z. T. Lewis, D. A. Mills

The composition of an infant’s gut microbiome can impact their immediate and long-term health. Bifdobacteria play a major role in structuring the gut microbiome of breastfed infants due to their ability to consume oligosaccharides found in human milk. However, recent studies have revealed that bifidobacteria are often absent in the gut microbiome of breastfed infants in some locations. 

This lack of colonization may be due either to differences in the environmental conditions in the gastrointestinal tract of uncolonized infants which prohibit the growth of bifidobacteria or a dearth of sources from which infants may acquire these specialized bacterial species. Potential mechanisms by which these broad factors may lead to lower colonization of infants by bifidobacteria are discussed herein. 

Environmental conditions which may select against bifidobacteria include low rates/duration of breastfeeding, milk glycan composition, and antimicrobial use. Routes of colonization by bifidobacteria which may be disrupted include maternal transfer via vaginal birth, fecal-oral routes, or via breast milk itself. A careful contemplation of the conditions experienced by bifidobacteria over human evolutionary history may lead to further hypotheses as to the causative factors of the differential colonization by this foundation genus in some contemporary locations.

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