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Establishment of the Gut Microbiota in Infancy

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Establishment of the Gut Microbiota in Infancy Establishment of the gut microbiota in infancy Ia Adlerberth Clinical bacteriology, Dept. Infectious diseases Sahlgrenska Academy, University of Göteborg The gut microbiota may have profound effects on the host • Effects on the host´s immune system • Effects on the host´s metabolism • Effects on the host´s central nervous system The gut microbiota may be involved in the development of a number of conditions and disease states Irritable bowel syndrome Inflammatory bowel disease allergy Celiac disease metabolic syndrome obesity Autism spectrum disorders atherosclerosis The gut microbiota may have profound effects on the immune system of the host Germfree animals: • Few (1/10) IgA-producing plasmacells in the gut mucosa • Few T-lymphocytes in the gut mucosa • Low levels of serum-IgG and serum-IgA • Reduced capacity to develop immunological tolerance to harmless antigens (e.g. ovalbumin) Does the early gut microbiota composition influence the risk of allergy development? Microbiota of the gastrointestinal tract Distal ileum 105-8 bacteria/ml Stomach Lactobacilli, streptococci <102 bacteria/ml E. coli, other enterobacteria Helicobacter pylori (laktobacilli) Bacteroides (streptococci) Clostridium Colon Duodenum, jejunum 1011 bacteria/g <105 bacteria/ml streptococci, lactobacilli, Granulicatella, Neisseria Veillonella The colonic microbiota 1/2-1 kg 1014 bacteria hundreds of species >99% anaerobic bacteria <50% belong to identified culturable species The colonic microbiota Phylum Genera Firmicutes Eubacterium, Ruminicoccus, Clostridium, Coprococcus, Blautia, Anaerostipes, Roseburia, Dorea, Butyrivibrio, Bryantella, Lachnobacterium, Lachnospira, Faecalibacterum, Anaerotruncus, Oscillospira, Papillibacter, Subdoligranulum, Sporobacter, Megasphaera, Veillonella, Dialister, Finegoldia, Peptostreptococcus, Streptococcus, Enterococcus Bacteroidetes Bacteroides, Parabacteroides, Alistipes, Prevotella, Butyricimonas, Odoribacter, Porphyromonas Actinobacteria Bifidobacterium, Collinsella, Egghertella Fusobacteria Fusobacterium, Leptotrichia Proteobacteria E. coli, Oxalobacter Verrucomicrobia Akkermansia muciniphila The gut microbiota Adults • A highly complex ecological system hundreds of species • Dominance of anaerobic bacteria (1000:1) • The majority of gut anaerobes has not yet been cultured Newborn infants • A less compex ecological system • Initially few species, increases over time • Initial proliferation of facultative bacteria • Fewer unculturable bacteria Acquisition of a complex microflora 11 facultatives anaerobes 10 Ruminococcus Akkermansia Eubacterium x 1000 Clostridium Faecalibacterium 7 Bacteroides 10 Peptostreptococcus Bifidobacterium Fusobacterium non-culturable bacteria Streptococcus Anaerostipes Veillonella Staphylococcus Lachnospira hundreds of species Enterococcus Lactobacillus Coprococcus E. coli , enterobacteria Roseburia Population Population counts 1 wk 1 mo 1 yr adult Age A complex ”adult-type” microflora is acquired at some years of age What determines which bacteria will establish in the gut microbiota? • which bacteria are the infant exposed to? • which bacteria manage to colonize, expand and persist in the gut microbiota? (selection) Sources of bacterial exposure bacterial environment close contacts load animals breastmilk other feeds mother Enviromental bacterial exposure The early gut microbiota differ between infants born in developing and industrialized societies Colonization by E. coli in the first days of life Lahore, Pakistan Göteborg, Sweden 100 100 80 80 60 60 40 40 % koloniserade 20 20 % koloniserade 0 0 1 2 3 4 days 1 2 3 4 days Adlerberth et al. Acta Paediatr 1991 Differences in gut colonization pattern between infants in different countries Sweden - Pakistan • Earlier colonization by E. coli and other enterobacteria, and a more diverse enterobacterial flora in Pakistani neonates Adlerberth et al. 1991 Sweden - Ethiopia • Earlier colonization by lactobacilli, E. coli and other enterobacteria, and enterococci in Ethiopian neonates • More staphylococci in Swedish neonates Bennet et al. 1991 Sweden - Estonia • Earlier colonization by lactobacilli and Eubacterium in Estonia • More clostridia, especially Clostridium difficile in Swedish one year old infants. Sepp et al. 1997, 1999 Sweden – UK – Germany – Spain - Italy South-North gradient: South: More Bacteroides, enterobacteria and lactobacilli in 6-week-old infants. North: More bifidobacteria, Atopobium, C. perfringens + C. difficile Fallani et al. 2010 Changing colonization pattern in Western countries? Colonization by E. coli 100 80 60 % colonized % 40 Sweden, England, Italy* Adlerberth et al. 2007 20 Studies from Western countries 1975-1989 Pakistan 1983 Adlerberth et al. 1991 3 7 14 28d 2mo 6mo 12mo *236 vaginally delivered infants born 1998-2002, ALLERGYFLORA Changing colonization pattern in Western countries? Less ”turn-over” of E. coli-strains in the gut microbiota today? Sweden, 1998-2001 2.1 E. coli-strains/12 months Nowrouzian et al. 2003 Sweden, 1980s 4.2 strains/11-18 months Kühn et al. 1986 Pakistan, 1980s 8.5 strains/6 months Adlerberth et al. 1998 0 6 12 18 months age Bacteria stimulate the immune system only when first colonizing the gut Secretory-IgA produced in response to the bacteria will plasma coat the bacteria and prevent cells further translocation over the gut mucosa S-IgA Shroff et al., Infect. Immun, 1995 Slow turn-over – little immune activation? Changing colonization pattern in Western countries? Colonization by Bacteroides 100 80 60 % colonized % 40 Sweden, England, Italy* Adlerberth et al. 2007 20 Studies from Western countries 1975-1989 Nigeria Rotimi et al. 1985 7 14 28d 2mo 6mo 12mo *236 vaginally delivered infants born 1998-2002, ALLERGYFLORA Changing colonization pattern in Western countries? Staphylococci, classical skin bacteria, colonize in the absence of competition from ”true” gut bacteria 100 80 60 40 % koloniserade % CoNS 1975-1989 CoNS Sweden, England, Italy* 20 S. aureus Sweden, England, Italy* S. aureus 1975-1989 3 7 14 28d 2mo 6mo 12mo *236 vaginally delivered infants born 1998-2002, ALLERGYFLORA Adlerberth et al. JACI 2007 S. aureus attain relatively high counts in the early gut microbiota And may persist for several months… 73% of strains were resident (>3w) Median persistence: 17weeks Lindberg E et al. Pediatr Res. 2000 Dec;48(6):741-7 Changing colonization pattern in Western countries? C. difficile in the gut microbiota of Swedish infants - indicating ”immaturity” of the gut microbiota? Unpublished data removed The modern Western colonization pattern 100 Late colonization by ”classical” gut 80 microbes like E. coli och Bacteroides 60 Bacteroides little exposure to faecal bacteria % colonized 40 E. coli in modern Western societies? 20 7d 2mo 6mo 12mo 100 Staphylococci are the first 80 colonizers and persist for many 60 months in the infantile gut % colonized 40 absence of competition from CoNS 20 S. aureus ”classical” gut microbes? 7d 2mo 6mo 12mo Frequent colonization by C. difficile sign of an ”immature” gut microbiota? Influence of 87 sectio- and 237 vaginally delivered infants delivery mode on ALLERGYFLORA Sweden, England, Italy gut colonization pattern Vaginal delivery Caesaean section E. coli Bacteroides bifidobacteria 100 100 100 80 80 80 60 60 60 40 40 40 20 20 20 P< 0.001 P< 0.001 P< 0.001 0 0 0 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m Klebsiella other Enterobacteriaceae clostridia 100 100 100 80 80 80 60 60 60 40 40 40 Cumulative colonization (%) colonization Cumulative 20 20 20 P=0.003 P< 0.001 P< 0.001 0 0 0 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m Adlerberth et al. JACI 2007 anaerobes ALLERGYFLORA 10 facultatives 10 infants delivered by x 1000 caesarean section 107 had lower anaerobe/facultative ratio at 12 months age Population counts (p=0.040) Adlerberth et al. JACI 2007 1 wk 1 mo 1 yr adult Slower maturation of Age the gut microbiota in sectio-delivered infants Unpublished data removed Reduced diversity in the gut microbiota of infants delivered by caesaren section HE Jakobsson et al. Gut. 2014 Apr;63(4):559-66. Lower diversity in sectio-delivered infants at most time- points from 1 week to 1 year of age Reduced diversity especially within phylum Bacteroidetes In developing countries: Sectio delivered infants ”catch up” more rapidly Rotimi 1985, Adlerberth 1991, Bennet 1991 Nigerian neonates E. coli Bacteroides 100 100 80 80 60 60 40 vaginal 40 % colonized sectio 20 20 1 2 3 6 d 1 2 3 6 days Rotimi et al. 1985 Close human and animal contacts increase exposure to gut bacteria Influence of siblings on ALLERGYFLORA Sweden, England, Italy gut colonization pattern siblings (n=149) no siblings (n=175) Klebsiella other Enterobacteriaceae clostridia 100 100 100 80 80 80 60 60 60 40 40 40 20 20 20 P=0.01 P=0.02 P< 0.001 Cumulative Cumulative (%) 0 0 0 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m 3d 1w 2w 4w 8w 6m 12m Lower anaerobe/facultative ratio by 12m age in first-born children (p<0.001). Adlerberth et al. JACI 2007 Slower maturation of the gut microbiota in first-born infants? Unpublished data removed Having older siblings is associated with increased bacterial diversity and increased bacterial richness in the gut microbiota at 18 months of age Laursen et al. BMC Microbiol. 2015 Aug 1;15:154. Does out of home-day care influence gut colonization pattern? Thompson et al 2015, Front Cell Infect Microbiol. 2015 Feb 5;5:3. Exclusively breastfed and non-exclusively breastefed infants, sampled before and after the introduction of solid foods.
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