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clinical gastroenterology and hepatology 2019 17 231 242 inuence of early life diet and the environment on the microbiome tien s dong and arpana gupta vatche and tamar manoukin division ...

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                                                                               Clinical Gastroenterology and Hepatology 2019;17:231–242
            Influence of Early Life, Diet, and the Environment
            on the Microbiome
                             ,‡                         ,‡,§
            Tien S. Dong*       and Arpana Gupta*
            *Vatche and Tamar Manoukin Division of Digestive Diseases, University of California, Los Angeles, Los Angeles, California;
            ‡David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California; and §G. Oppenheimer Center
            for Neurobiology of Stress and Resilience, University of California, Los Angeles, Los Angeles, California
            Advances in sequencing technology and bioinformatics        disease models, such as obesity and irritable bowel syn-
            have greatly enhanced our ability to understand the hu-     drome (IBS), are discussed to highlight how environ-
            man microbiome. Over the last decade, a growing body        mental   perturbations    in  the   human microbiome
            of literature has linked nutrition and the environment to   contribute to disease.
            the microbiome and is now thought to be an important
            contributor to overall health. This paper reviews the          Environmental Factors
            literature from the past 10 years to highlight the influence
            of environmental factors such as diet, early life adversity
            and stress in shaping and modifying our microbiome to-         The environment plays a critical part in the compo-
            wards health and disease. The review shows that many        sition of the human microbiome (Figure 1). A total of
            factors such as the mode of delivery, breast milk, stress,  22%–36% of the interperson microbiome variability is
            diet and medications can greatly influence the develop-      associated with environmental factors and only 1.9%–
            mentofourgutmicrobiomeandpotentially make us more           9%bygenetics.2 Environmental factors start in the early
            prone to certain diseases. By incorporating environmental   days of life and extend well into adulthood. Next we
            factors into models that study the microbiome in the        highlight how environmental factors, such as the mode of
            setting of health and disease, may provide a better un-
            derstanding of disease and potentially new areas of treat-  delivery, breastfeeding, and introductions of foods, are
            ment. To highlight this, we will additionally explore the   critical steps in the development of a mature adult
            role of the environment and the microbiome in the devel-    microbiome. We later show how such environmental
            opment of obesity and functional bowel disorders.           factors as diet, smoking, home life, and stress can induce
                                                                        shifts in the microbiome during the lifespan and make
            Keywords: Gut Microbiome; Environment; Early Life Diet;     humans more prone to certain diseases.
            Stress; Obesity; Irritable Bowel Syndrome.
                                                                           Early Life Events
                 n the last decade, advances in sequencing technol-        Early life events are critical to the development of the
               Iogyandbioinformaticshave enhanced the ability to        humanmicrobiomebecausetheycanshapethesequence
            understand the human microbiome, and how the envi-          of microbial community establishment and ultimately the
            ronment contributes to shifts in these complex systems      final composition of the mature adult microbiome.6 This
            over time.1,2 The human microbiome represents a mi-         section summarizes how the microbiome matures during
            crobial community that encompasses 10 times more cells      the transition from inside the womb, which is a relatively
            andapproximately 100 times more genes than contained        sterile environment, into the external environment after
            in the human body alone.3 Although the major function       birth when ingestion of milk and solid food are intro-
            of the gut microbiome is to aid in the fermentation and     duced. Microbial community differences during each key
            energy extraction of indigestible dietary fiber, multiple    early life process are summarized in Table 1.
            studies have linked the microbiome to energy homeo-            Prenatal. Studies have suggested that the introduc-
            stasis, immune function, and the development of certain     tion of microbes can occur as early as during the prenatal
                     4
            diseases.  An increased understanding of the relation-      period. Although certain intrauterine infections and
            ship between humans, their microbes, and the environ-       bacteria   from     such    groups    as   Burkholderia,
            ment can help better understand the maintenance of
            health and the development of disease.5 This review
            explores the recent literature related to the influence of   Abbreviations used in this paper: C-section, cesarean section; IBS,
            environmental factors, such as early life events, diet,     irritable bowel syndrome; SCFA, short-chain fatty acid.
            pathogens, social factors, and stress, on the complex          Most current article
            host-microbe interactions and how these interactions                          ©2019bythe AGA Institute
            contribute to or are protective against disease. Example                          1542-3565/$36.00
                                                                                     https://doi.org/10.1016/j.cgh.2018.08.067
              232    Dong and Gupta                                                              Clinical Gastroenterology and Hepatology Vol. 17, No. 2
              Figure 1. Environmental factors shape and change the microbiome over time and perturbations can lead to disease. Maternal
              factors: vaginal infections and gut microbiome can lead to bacterial translocation into the uterus. Postnatal factors: mode of
              delivery, breastfeeding versus formula feeding, introduction of solid food, and early life adversity and antibiotic exposure can
              shape the developing microbiome in early childhood. Environmental factors across the lifespan: long-term diet and exposure
              to animals can modify the microbiome throughout childhood and adulthood. Perturbations to the microbiome: medications,
              suchasantibiotics, proton pump inhibitors, and metformin, and a variety of different diets can make individuals more prone to
              disease, such as inflammatory bowel disease, IBS, and obesity. Stress can lead to changes in the microbiome that affects
              intestinal permeability and SCFA production. Smoking can cause microbial shifts that change inflammatory signaling and
              colonic mucin production, all of which can be mechanisms that lead to the development of disease.
              Actinomycetales, and Alphaproteobacteria are associated                abundant phyla isolated from first-pass meconium were
              withpretermdelivery,ithasbeenshownthatavarietyof                       Firmicutes, Proteobacteria, and Bacteriodetes.10 All bac-
              other microbes may be present in the placenta, umbilical               teria isolated from the umbilical cord blood of healthy
              cord, amniotic fluid, and meconium of normal preg-                      neonates belonged to the genus Enterococcus, Strepto-
                      7–9                                                                                                                    11
              nancy.      Thematernal microbiome is likely translocated              coccus, Staphylococcus,orPropionibacterium.                 In the
              into the uterus via the bloodstream, an idea supported by              placenta, the genus Bifidobacterium and Lactobacillus
              the detection of labeled Enterococcus faecium in the                   were identified.8
              meconium of inoculated pregnant mice.7 In a recent                         However, the role and function of these microbes in
              population-based study, researchers found the most                     human health or disease during the prenatal period re-
                                                                                     mains unclear. Because of the possibility of maternal
                                                                                     contamination, it is difficult to definitively establish the
                                                                                     presence of a prenatal microbiome.12 Further studies are
              Table 1.Microbial Communities Described by Type of Early               required     to    confirm the existence of a viable
                        Life Environmental Factors
                                                                                     intrauterine-resident       microbiota      with    the    use    of
                                                   Bacterial                         adequate controls (such as maternal blood or sampling
                Environmental factors             community          References      at a site nearby delivery) to determine if the existence of
              Vaginal delivery vs             [Lactobacillus             18,19       such a microbiome might affect the future development
                  cesarean section delivery   [Prevotella                            of the newborn.
                                              [Sneathia                                  Delivery. Although the existence of a prenatal micro-
                                              [Bifidobacterium                        biome may be controversial, many agree that the first
                                              [Bacteroides                           major introduction of a microbial community to a
                                              YStaphylococcus                        newborn is through delivery.6 As the newborn is passing
                                              YPropionibacterium                     through the vaginal canal, it is ultimately introduced to
                                              YCorynebacterium
              Breastfeeding vs                [Bifidobacteria             31,32       the commensal vaginal and fecal microbiome of the
                  formula feeding             [Lactobacillus                         mother.13 This community of microbes seems to be
                                              YClostridiales                         distinct from the community of nonpregnant women
                                              YProteobacteria                        because the vaginal microbiome changes during preg-
              Introduction of solid food      [Lachnospiraceae           35,36       nancy.14 For example, healthy pregnant women, when
                                              [Ruminococcaceae
                                              [Bacteroidaceae                        compared with nonpregnant women, had lower vaginal
                                              YLactobacillaceae                      bacterial diversity with higher levels of Lactobacillus,
                                              YBifidobacterium                        Clostridiales, Bacteroidales, and Actinomycetales; these
                                              YEnterococcaceae                       levels were associated with gestational age.15 Beyond
                                              YEnterobacteriaceae                    the vaginal microbiome, there is also evidence that the
                                                                                     community of the maternal gut also changes during the
             January 2019                                                                     The Environment Impacts the Microbiome   233
             course of pregnancy. For example, a Finnish cohort of           studies demonstrated that the direct mother-to-infant
             91 healthy pregnant women demonstrated decreased                transmission changes over time as different floras are
             bacterial diversity as evidenced by increased levels of         introduced through processes, such as skin contact and
             high-energy-yielding fecal microbiota with increasing           breastfeeding.23,24
             gestational age.16 From the first to the third trimester,            Breastfeeding and introduction of solid food. The
             the proportion of Proteobacteria, including species of the      other major early life events that affect the development
             Enterobacteriaceae family and Streptococcus genus,              and maturation of the newborn microbiome are breast-
             decreased, whereas the proportion of Faecalibacterium           feeding and the introduction of solid food. Breast milk
             prausnitzii increased. These changes in the microbiome          bacteria, such as Corynebacterium and Rothia, can seed
             were independent of prepregnancy body weight, gesta-            the infant gut and influence the bacteria that follows,
                                                                                                                                        25
             tional diabetes, diet, and antibiotic use, suggesting that      affecting the communities even through adulthood.
             they were caused by the changes of normal pregnancy.            These early seeding events may be the mechanism by
             These changes in the microbiome have a beneficial role           which breast milk can protect children against autoim-
             for the mother and neonate by protecting against certain        mune diseases, such as asthma and type 1 diabetes.26
             infections, such as Neisseria gonorrhea and bacterial               Similar to the vaginal microbiome, it has been shown
             vaginosis, and also by permitting greater efficiency for         that the microbiome of breast milk also varies with
             energy harvest to support the growth of the mother and          increasing gestational age, and is related to maternal
             fetus.16,17                                                     health and mode of delivery.26,27 The breast milk mi-
                With    these    specific   pregnancy-related     changes     crobial community is dominated by Corynebacterium,
             effecting the vaginal and fecal microbiome of the mother,       Ralstonia, Staphylococcus, Streptococcus, Serratia, Pseu-
             it is unsurprising that the mode of delivery also greatly       domonas, Propionibacterium, Sphingomonas, and Bra-
             affects how the newborn microbiome develops. The dif-           dyrhizobiaceae.26 In a study of 107 healthy women who
             ferences seen between cesarean section (C-section) and          were breastfeeding their infants for the first 30 days of
             vaginally delivered babies are drastic. Compared with           life, the gut microbiome changed in a dose-dependent
             vaginally born babies, those that are born by C-section         manner with 27.7% of the mean bacteria being derived
             without membrane rupture have no vaginal microbes,              from breast milk and 10.3% from areola skin.26
             such as Lactobacillus, Prevotella, and Sneathia. Instead,           Breast milk also contains many important prebiotic
             babies born by C-section are colonized with skin mi-            compounds, such as human milk oligosaccharides. These
             crobes, such as Staphylococcus, Propionibacterium, and          sugar polymers are almost exclusively metabolized by
             Corynebacterium.18 These babies have a delayed coloni-          the gut microbiome28 and they can promote the growth
             zation of intestinal microbes, such as Bacteroides and          of key communities including Bifidobacterium spp.29
             Bifidobacterium.19 Although the exact length of time             Bifidobacteria has been shown to inhibit the growth of
             these differences exist is unknown, microbial differences       pathogenic organisms and improve barrier function in
             between C-section and vaginally delivered babies have           the infant gut.30 In a mouse model, human milk oligo-
             been observed to as far out as 7 years of age.20 The            saccharides were found to be protective in the develop-
             deficits in the human microbiome associated with                 ment of autoimmune disease and obesity.31,32
             C-section deliveries have been implicated in certain                There are clear differences in the composition of the
             childhood autoimmune disease, such as celiac disease,           microbiome in infants who are breastfed versus those
             asthma, and type I diabetes.21 These studies also suggest       who are formula fed. Infants who are breastfed have a
             that restoration of a more “normal” microbiome after            higher proportion of Bifidobacterium and Lactobacillus
             C-section deliveries may therefore be beneficial. “Vaginal       spp, whereas infants who are formula-fed have a higher
             seeding,” or the process by which vaginal fluids are             proportion    of  Clostridiales   and Proteobacteria.33,34
             applied to a newborn child delivered by C-section, has          Formula-fed infants also have lower diversity and rich-
             been a method used to restore the human microbiome.             ness even after the first year of life as compared with
             Although a small pilot study of 4 babies demonstrated           their breastfed counterparts.33 In a study of 30 preterm
             the feasibility of restoring the early microbiome of babies     infants, breastfeeding was found to be protective against
             born by C-section,22 the long-term health consequence of        gut immaturity and possibly necrotizing enterocolitis.35
             such a procedure remains unknown and may even in-               Several other epidemiologic studies have provided sup-
             crease the risk of transmittable diseases to the newborn.       port for the beneficial role of breastfeeding in the
             Therefore, further prospective studies are needed to            development of disease. Formula feeding has been
             determine the safety and potential benefits, if any, of          associated with various inflammatory and autoimmune
             these methods used to restore the human microbiome.             diseases.36 In contrast, breastfeeding, through its effects
                Even though the mode of delivery is important to             onthemicrobiome,hasbeenassociatedwithaprotective
             microbial seeding, it may not be the only mode for ver-         role against asthma, autism spectrum disorder, and type
             tical transmission. Recent human studies have high-             1 diabetes.26,36
             lighted maternal vertical transmission from multiple                One of the last major events in early life affecting mi-
             different sources, such as the skin, mouth, and gastro-         crobial development is the introduction of solid food.
             intestinal track.23,24 By examining strain-level data, these    Although breast milk keeps the microbiome in a state that
             234   Dong and Gupta                                                     Clinical Gastroenterology and Hepatology Vol. 17, No. 2
             is characterized by low diversity and Bifidobacterium              Diet
             predominance, the introduction of solid food and the
             cessation of breastfeeding increases adult-associated mi-         During the early stages of life, breast milk and the
                                                                       37
             crobes, such as Lachnospiraceae and Ruminococcaceae.           introduction of solid food are critical events in the
             In a Danish study of 330 children between 9 and 36             development of the human microbiome. Therefore, it is
             months of age, Lactobacillaceae,        Bifidobacteriaceae,     not surprising that the introduction of diet throughout
             Enterococcaceae,    and    Enterobacteriaceae    decreased,    life has large effects on the human microbiome. The gut
             whereas Lachnospiraceae, Ruminococcaceae, and Bacter-          microbiota can change within days of a new diet, but to
             oidaceae increased during the period when solid foods          what extent these changes are permanent once the new
                                     38                                                                               48
             was being introduced.      Another study of 531 children       diet has terminated remains uncertain.       In this section,
             born in 5 different countries showed similar results in-       we review the current literature, focusing on popular
             dependentoflocation, use of antibiotics, mode of delivery,     diets and how the microbiome is connected (summarized
             or milk feeding practices, suggesting that these changes       in Table 2).
             were typical of the normal developing microbiome as               Westerndiet. The Western diet or standard American
                                                  39                        diet is a diet characterized by high fat, high sugar, high
             solid foods are being introduced.        This transition is
             necessary and beneficial. It allows for a microbial com-        level of red and processed meat, high levels of refined
             munity that is better equipped to extract energy and           grains, and a lower level of fiber.48 Many studies have
             process a diet that is no longer dependent on milk to a        linked the Western diet to inflammation, diabetes, car-
             diet that is higher in fiber and protein, similar to the diet   diovascular risks, obesity, and metabolic syndrome.48,49
             of a mature adult.                                             Although a Western diet affects many different cell
                Early life adversity. Recently, researchers are discov-     types, such as adipocytes, immune cells, and endocrine
             ering that early life adverse events can manipulate the        cells, there is also a strong link that connects the dele-
             microbial community in significant ways. In rats, limited       terious effects of a Western diet to shifts in the micro-
             nesting stress during postnatal days 2–10 led to a             biome.48 Compared with other indigenous diets, the
             delayed   maturation     of  the   hypothalamic-pituitary-     microbiome on a Western diet is characterized by a
             adrenal axis that was associated with decreased micro-         significantly lower microbial diversity and species rich-
             bial diversity, an increase of gram-positive cocci, and a      ness.50 The Western diet microbial composition is clas-
             reduction of fiber-degrading bacteria.40 Similar findings        sically characterized by an overabundance of the phyla
             were demonstrated in mice and rhesus monkeys when              Firmicutes and a decrease in Bacteroidetes.51 On a genus
             exposed to stress at an early age.41,42 Finally, in patients   level, a Western diet shows a decrease in Bifidobacterium
             with IBS, those that had a microbiome profile distinct          and Lactobacillus, whereas being high in Enterobacter.52
             from healthy control subjects were more likely to have a       Consequently, the Western diet has been linked to an
             history of early adverse events and trauma than those          increase in endotoxemia, a state characterized by
             with a microbiome that was more similar to healthy             decreasedintestinal barrier function and increased levels
             control subjects.43 Although these studies are predomi-        of   bacterial  lipopolysaccharides     and inflammatory
             nantly associations, exploring how adverse events and          signaling.53,54 Furthermore, a Western diet can possibly
             early gut dysbiosis can cause such diseases as IBS is an       lead to permanent microbiome changes that may be
             active research area.                                          responsible for postdieting weight regain or the common
                Antibiotic use can also play a significant role during       concept of yo-yo dieting, which has been linked to higher
             early life. The average U.S. child receives about 1–3          long-term weight gain, increased obesity-related risk
             antibiotic courses by the age of 2 years.44 Several studies                                                        55
                                                                            factors, and increased difficulty reducing weight.
             have highlighted how antibiotic exposure in children can          Mediterranean diet. In contrast to a Western diet, a
             beassociated with an increased risk for obesity, diabetes,     Mediterranean diet is considered a healthier diet. It is
             allergies, asthma, IBS, and inflammatory bowel dis-             characterized by a beneficial fatty acid profile; higher
             ease.33,45 Children exposed to antibiotics have delayed        intake of fiber, vegetables, and fruits; and with lower
             maturation of their microbiome as compared with their          intake of sugar and red meat.56 A recent study demon-
             respective control subjects, but whether this is the exact     strated that out of 153 participants, those who were
             mechanism by which early antibiotics predisposes chil-         more adherent to a Mediterranean diet had an increased
             dren to disease is still unclear.33 In animal models, per-     level of short-chain fatty acids (SCFA), Prevotella, and
             ipartum antibiotic exposure in the mother can lead to          certain Firmicutes, which have all been associated with
             persistent gut dysbiosis in the offspring and colitis in       decreased cardiovascular events.57 Additionally, they
             susceptible individuals.46,47 Although these studies do        also showed that low adherence to the Mediterranean
             not provide an exact mechanistic explanation of the ef-        diet led to decreases in urinary trimethylamine oxide
             fect of antibiotic use on microbiome development or on         levels, which is associated with higher cardiovascular
             disease susceptibility, they do highlight that early anti-     risk.57,58 Several studies have shown that consumption of
             biotic exposure is linked in some way to the normal            foods encompassing the typical Mediterranean diet
             development of microbial community and to disease              improved obesity, inflammation, and lipid profile and
             development.                                                   were    associated    with   increases   in   Lactobacillus,
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...Clinical gastroenterology and hepatology inuence of early life diet the environment on microbiome tien s dong arpana gupta vatche tamar manoukin division digestive diseases university california los angeles david geffen school medicine g oppenheimer center for neurobiology stress resilience advances in sequencing technology bioinformatics disease models such as obesity irritable bowel syn have greatly enhanced our ability to understand hu drome ibs are discussed highlight how environ man over last decade a growing body mental perturbations human literature has linked nutrition contribute is now thought be an important contributor overall health this paper reviews environmental factors from past years adversity shaping modifying plays critical part compo wards review shows that many sition figure total mode delivery breast milk interperson variability medications can develop associated with only mentofourgutmicrobiomeandpotentially make us more bygenetics start prone certain by incorpor...

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