Determinants of the human infant intestinal microbiota after the introduction of first complementary foods in infant samples from five European centres
TL;DR: The faecal microbiota of infants after first complementary foods was different to that before weaning commenced, many of the initial influences on microbiota composition were still evident.
Abstract: Although it is well established that early infant feeding has a major influence on the establishment of the gut microbiota, very little is understood about how the introduction of first solid food influences the colonization process. This study aimed to determine the impact of weaning on the faecal microbiota composition of infants from five European countries (Sweden, Scotland, Germany, Italy and Spain) which have different lifestyle characteristics and infant feeding practices. Faecal samples were collected from 605 infants approximately 4 weeks after the introduction of first solid foods and the results were compared with the same infants before weaning (6 weeks of age) to investigate the association with determining factors such as geographical origin, mode of delivery, previous feeding method and age of weaning. Samples were analysed by fluorescence in situ hybridization and flow cytometry using a panel of 10 rRNA targeted group- and species-specific oligonucleotide probes. The genus Bifidobacterium (36.5 % average proportion of total detectable bacteria), Clostridium coccoides group (14 %) and Bacteroides (13.6 %) were predominant after weaning. Similar to pre-weaning, northern European countries were associated with a higher proportion of bifidobacteria in the infant gut microbiota while higher levels of Bacteroides and lactobacilli characterized southern European countries. As before weaning, the initial feeding method influenced the Clostridium leptum group and Clostridium difficile+Clostridium perfringens species, and bifidobacteria still dominated the faeces of initially breast-fed infants. Formula-fed babies presented significantly higher proportions of Bacteroides and the C. coccoides group. The mode of birth influenced changes in the proportions of bacteroides and atopobium. Although there were significant differences in the mean weaning age between countries, this was not related to the populations of bifidobacteria or bacteroides. Thus, although the faecal microbiota of infants after first complementary foods was different to that before weaning commenced, many of the initial influences on microbiota composition were still evident.
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TL;DR: The complex interplay between the gut microbiota, diet and health is considered and better definition of those dominant commensal bacteria, community profiles and system characteristics that produce stable gut communities beneficial to health is important.
Abstract: The microbial communities that colonize different regions of the human gut influence many aspects of health. In the healthy state, they contribute nutrients and energy to the host via the fermentation of nondigestible dietary components in the large intestine, and a balance is maintained with the host's metabolism and immune system. Negative consequences, however, can include acting as sources of inflammation and infection, involvement in gastrointestinal diseases, and possible contributions to diabetes mellitus and obesity. Major progress has been made in defining some of the dominant members of the microbial community in the healthy large intestine, and in identifying their roles in gut metabolism. Furthermore, it has become clear that diet can have a major influence on microbial community composition both in the short and long term, which should open up new possibilities for health manipulation via diet. Achieving better definition of those dominant commensal bacteria, community profiles and system characteristics that produce stable gut communities beneficial to health is important. The extent of interindividual variation in microbiota composition within the population has also become apparent, and probably influences individual responses to drug administration and dietary manipulation. This Review considers the complex interplay between the gut microbiota, diet and health.
1,766 citations
10 Jan 2019
TL;DR: This review will provide an overview of the studies that focus on gut microbiota balances in the same individual and between individuals and highlight the close mutualistic relationship between gut microbiota variations and diseases.
Abstract: Each individual is provided with a unique gut microbiota profile that plays many specific functions in host nutrient metabolism, maintenance of structural integrity of the gut mucosal barrier, immunomodulation, and protection against pathogens. Gut microbiota are composed of different bacteria species taxonomically classified by genus, family, order, and phyla. Each human’s gut microbiota are shaped in early life as their composition depends on infant transitions (birth gestational date, type of delivery, methods of milk feeding, weaning period) and external factors such as antibiotic use. These personal and healthy core native microbiota remain relatively stable in adulthood but differ between individuals due to enterotypes, body mass index (BMI) level, exercise frequency, lifestyle, and cultural and dietary habits. Accordingly, there is not a unique optimal gut microbiota composition since it is different for each individual. However, a healthy host–microorganism balance must be respected in order to optimally perform metabolic and immune functions and prevent disease development. This review will provide an overview of the studies that focus on gut microbiota balances in the same individual and between individuals and highlight the close mutualistic relationship between gut microbiota variations and diseases. Indeed, dysbiosis of gut microbiota is associated not only with intestinal disorders but also with numerous extra-intestinal diseases such as metabolic and neurological disorders. Understanding the cause or consequence of these gut microbiota balances in health and disease and how to maintain or restore a healthy gut microbiota composition should be useful in developing promising therapeutic interventions.
1,502 citations
Cites background from "Determinants of the human infant in..."
...The abundance of genera Bifidobacterium, Clostridium coccoides, and Bacteroides are predominant after weaning [40]....
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...Over 70 Bifidobacteriaceae↓ Clostridium *↓ Proteobacteria *↑ ↓ [40]...
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...[40] demonstrated that northern European countries are associated with a higher proportion of Bifidobacteria in the infant gut microbiota, whereas higher levels of Bacteroides and Lactobacilli characterize southern European countries....
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TL;DR: How glycans shape the composition of the gut microbiota over various periods of time is described, the mechanisms by which individual microorganisms degrade these glycans, and potential opportunities to intentionally influence this ecosystem for better health and nutrition are described.
Abstract: In this Review, Martens and colleagues describe how dietary and endogenous glycans shape the composition of the gut microbiota and how individual microorganisms degrade these glycans. They also highlight the potential to influence this ecosystem for better health and nutrition.
1,048 citations
TL;DR: The infant microbiota, the mechanisms that drive its establishment and composition, and how microbial consortia may be molded by natural or artificial interventions are described and the relevance of key microbial players of the infant gut microbiota, in particular bifidobacteria, with respect to their role in health and disease are discussed.
Abstract: The human gut microbiota is engaged in multiple interactions affecting host health during the host's entire life span. Microbes colonize the neonatal gut immediately following birth. The establishment and interactive development of this early gut microbiota are believed to be (at least partially) driven and modulated by specific compounds present in human milk. It has been shown that certain genomes of infant gut commensals, in particular those of bifidobacterial species, are genetically adapted to utilize specific glycans of this human secretory fluid, thus representing a very intriguing example of host-microbe coevolution, where both partners are believed to benefit. In recent years, various metagenomic studies have tried to dissect the composition and functionality of the infant gut microbiome and to explore the distribution across the different ecological niches of the infant gut biogeography of the corresponding microbial consortia, including those corresponding to bacteria and viruses, in healthy and ill subjects. Such analyses have linked certain features of the microbiota/microbiome, such as reduced diversity or aberrant composition, to intestinal illnesses in infants or disease states that are manifested at later stages of life, including asthma, inflammatory bowel disease, and metabolic disorders. Thus, a growing number of studies have reported on how the early human gut microbiota composition/development may affect risk factors related to adult health conditions. This concept has fueled the development of strategies to shape the infant microbiota composition based on various functional food products. In this review, we describe the infant microbiota, the mechanisms that drive its establishment and composition, and how microbial consortia may be molded by natural or artificial interventions. Finally, we discuss the relevance of key microbial players of the infant gut microbiota, in particular bifidobacteria, with respect to their role in health and disease.
970 citations
Cites background from "Determinants of the human infant in..."
...During weaning, due to the complementary introduction of a variety of novel food substances and nutrients, the alpha diversity increases, resulting in the replacement of Proteobacteria and Actinobacteria by Firmicutes and Bacteroidetes phyla as the dominant members of the infant microbiota (112, 113)....
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TL;DR: This review provides a systematic overview and detailed references of the total of 1057 intestinal species of Eukarya, Archaea and Bacteria based on the phylogenetic framework of their small subunit ribosomal RNA gene sequences and unifies knowledge about the prevalence, abundance, stability, physiology, genetics and the association with human health of these gastrointestinal microorganisms.
Abstract: The microorganisms that inhabit the human gastrointestinal tract comprise a complex ecosystem with functions that significantly contribute to our systemic metabolism and have an impact on health and disease. In line with its importance, the human gastrointestinal microbiota has been extensively studied. Despite the fact that a significant part of the intestinal microorganisms has not yet been cultured, presently over 1000 different microbial species that can reside in the human gastrointestinal tract have been identified. This review provides a systematic overview and detailed references of the total of 1057 intestinal species of Eukarya (92), Archaea (8) and Bacteria (957), based on the phylogenetic framework of their small subunit ribosomal RNA gene sequences. Moreover, it unifies knowledge about the prevalence, abundance, stability, physiology, genetics and the association with human health of these gastrointestinal microorganisms, which is currently scattered over a vast amount of literature published in the last 150 years. This detailed physiological and genetic information is expected to be instrumental in advancing our knowledge of the gastrointestinal microbiota. Moreover, it opens avenues for future comparative and functional metagenomic and other high-throughput approaches that need a systematic and physiological basis to have an impact.
857 citations
Cites background from "Determinants of the human infant in..."
...Based on the literature data, it can be concluded that Atopobium spp. are among the earliest colonizers of the human intestinal tract as they are reported to be present in gastrointestinal contents of 6-week-old infants (Fallani et al., 2011)....
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References
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TL;DR: In this review, the development of the intestinal microbiota is discussed in terms of initial acquisition and subsequent succession of bacteria in human infants and the advantages of modern molecular ecology techniques that provide sensitive and specific, culture-independent evaluation of the gastrointestinal ecosystem are introduced.
1,304 citations
"Determinants of the human infant in..." refers result in this paper
...11 On: Thu, 04 Jul 2019 18:14:04 suggesting that the effect of early antibiotic administration will fade rather than persist upon weaning even after the treatment has stopped, as formerly reported (Mackie et al., 1999)....
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...This effect disappeared after weaning started, 1390 Microbiology 157 suggesting that the effect of early antibiotic administration will fade rather than persist upon weaning even after the treatment has stopped, as formerly reported (Mackie et al., 1999)....
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TL;DR: It is shown for the first time that the primary gut flora in infants born by cesarean delivery may be disturbed for up to 6 months after the birth, and even longer follow-up is needed to establish how long-lasting these alterations of thePrimary gut flora can be.
Abstract: Background:Newborn infants in modern maternity hospitals are subject to numerous factors that affect normal intestinal colonization-for example, cesarean delivery and antimicrobial agents. To study the duration of the effect of external factors on intestinal colonization, two groups of infan
880 citations
"Determinants of the human infant in..." refers background in this paper
...Grönlund et al. (1999) studied 30 infants delivered by Caesarean section whose mothers had received antibiotics and 34 vaginally delivered infants, and observed a delay in faecal colonization and low Bacteroides in the Caesarean group during the first 6 months of life, even after weaning....
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TL;DR: At 12 months, the anaerobic bacterial populations of the large bowel of breast-fed and formula-fed infants were beginning to resemble those of adults in number and composition and there was a corresponding decrease in the number of facultative anaerobes.
Abstract: The succession of bacterial populations in the large bowel of seven breast-fed and seven formula-fed infants was examined during the first year of life. The composition of the intestinal microflora varied according to the infant's diet. During the first week of life breast-fed and formula-fed infants were colonised by enterobacteria and enterococci followed by bifidobacteria, Bacteroides spp., clostridia and anaerobic streptococci. From week 4 until solid foods were given, breast-fed babies had a simple flora consisting of bifidobacteria and relatively few enterobacteria and enterococci. Formula-fed babies during the corresponding period were more often colonised by other anaerobes in addition to bifidobacteria and had higher counts of facultatively anaerobic bacteria. The introduction of solid food to the breast-fed infants caused a major disturbance in the microbial ecology of the large bowel as counts of enterobacteria and enterococci rose sharply and colonisation by Bacteroides spp., clostridia and anaerobic streptococci occurred. This was not observed when formula-fed infants began to take solids; instead, counts of facultative anaerobes remained high while colonisation by anaerobes other than bifidobacteria continued. At 12 months, the anaerobic bacterial populations of the large bowel of breast-fed and formula-fed infants were beginning to resemble those of adults in number and composition and there was a corresponding decrease in the number of facultative anaerobes. These changes are discussed in relation to changes in susceptibility to gastro-intestinal infection.
588 citations
"Determinants of the human infant in..." refers result in this paper
...In the present study, C. difficile and C. perfringens also significantly decreased after weaning in accordance with previous observations (Stark & Lee, 1982; Benno et al., 1984; Fallani et al., 2006)....
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...Pre-weaning breastfeeding was still associated with higher proportions of bifidobacteria, while formula feeding was characterized by higher proportions of Bacteroides and C. coccoides in accordance with previous studies (Stark & Lee, 1982; Hopkins et al., 2005)....
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TL;DR: Delivery mode and feeding method influenced the fecal microbiota of European infants at 6 weeks, as expected, but the effect of country of birth was more pronounced, with dominant bifidobacteria in northern countries and greater early diversification in southern European countries.
Abstract: OBJECTIVES: There are many differences in diet and lifestyle across Europe that may influence the development of the infant gut microbiota. This work aimed to assess the impact of geographic area, mode of delivery, feeding method, and antibiotic treatment on the fecal microbiota of infants from 5 European countries with different lifestyle characteristics: Sweden, Scotland, Germany, Italy, and Spain. PATIENTS AND METHODS: Fecal samples from 606 infants (age 6 weeks) recruited within the European project INFABIO were analyzed by fluorescent in situ hybridization combined with flow cytometry using a panel of 10 rRNA targeted group- and species-specific oligonucleotide probes. Information on factors potentially affecting gut microbiota composition was collected with questionnaires and associations were evaluated with multivariate analyses. RESULTS: The Bifidobacterium genus was predominant (40% average proportion of total detectable bacteria), followed by Bacteroides (11.4%) and enterobacteria (7.5%). Northern European countries were associated with higher proportions of bifidobacteria in infant feces, whereas a more diverse microbiota with more bacteroides characterized southern countries. Bifidobacteria dominated the microbiota of breast-fed infants, whereas formula-fed babies had significantly higher proportions of Bacteroides and members of the Clostridium coccoides and Lactobacillus groups. Newborns delivered by cesarean section or from mothers treated with antibiotics perinatally had lower proportions of Bacteroides and members of the Atopobium cluster. CONCLUSIONS: Delivery mode and feeding method influenced the fecal microbiota of European infants at 6 weeks, as expected, but the effect of country of birth was more pronounced, with dominant bifidobacteria in northern countries and greater early diversification in southern European countries
517 citations
"Determinants of the human infant in..." refers background or methods or result in this paper
...…seen at 6 weeks of age (a gradient of high numbers of bifidobacteria in northern Europe to higher Bacteroides and lactobacilli in southern Europe) (Fallani et al., 2010) still persisted 4 weeks after first introduction of solid foods, particularly for Bacteroides, bifidobacteria and the C. leptum…...
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...We have previously reported the factors which affect the infant microbiota at 6 weeks of age (Fallani et al., 2010)....
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...At 6 weeks there was a marked effect of antibiotic treatment in infants or their mother perinatally (Fallani et al., 2010)....
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...The FISH method was carried out as described previously (RigottierGois et al., 2003a, b; Fallani et al., 2010) using a panel of 10 groupand species-specific probes covalently linked with indodicarbocyanine (Cy5) at their 59 end to assess the microbiota composition (Fallani et al., 2006)....
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...The majority of these infants (531 of 605) had been similarly studied at 6 weeks old (baseline measurement) and could therefore provide paired data (Fallani et al., 2010)....
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TL;DR: The results suggest a shift in the intestinal microflora among infants in western industrialized countries.
Abstract: The intestinal microflora of 1-y-old healthy Estonian (n = 27) and Swedish infants (n = 29) was studied by quantitative culture of faecal samples. The major differences were high counts of lactobacilli and eubacteria in the former and increased numbers of clostridia in the latter babies. Bifidobacteria and anaerobic cocci prevailed equally in both groups, while eubacteria and enterococci were the major microorganisms in many Estonian infants and bacteroides and clostridia in many Swedish infants. The microflora of the Estonian infants was in many aspects similar to the flora prevailing in infants of western Europe in the 1960s. The results suggest a shift in the intestinal microflora among infants in western industrialized countries.
427 citations
"Determinants of the human infant in..." refers background in this paper
...The few previous studies reported here considered the microbiota composition for only one or two countries and the majority investigated a small number of bacterial groups (George et al., 1996; Guérin-Danan et al., 1997; Sepp et al., 1997)....
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...The few previous studies reported here considered the microbiota composition for only one or two countries and the majority investigated a small number of bacterial groups (George et al., 1996; Guérin-Danan et al., 1997; Sepp et al., 1997)....
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