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Effect of fecal microbiota transplantation route of administration on gut colonization and host response in preterm pigs.

ABSTRACT: This study examined gut colonization patterns and host responses to fecal microbiota transplantation (FMT) by different administration routes after preterm birth. In two separate experiments, cesarean-delivered, preterm pigs were administered combined oral?+?rectal, or exclusively rectal donor feces, and compared with saline controls. After 5 days, stomach and colon bacterial compositions were determined by 16S rRNA gene amplicon sequencing, and organic acid metabolites measured. Further, gut pathology, mucosa bacterial adherence, and goblet cell density were assessed. FMT increased the relative abundance of obligate anaerobes in the colon without affecting total bacterial load. Bacteroides colonized recipients despite low abundance in the donor feces, whereas highly abundant Prevotella and Ruminococcaceae did not. Further, FMT changed carbohydrate metabolism from lactate to propionate production thereby increasing colonic pH. Besides, FMT preserved goblet cell mucin stores and reduced necrotizing enterocolitis incidence. Only rectal FMT increased the stomach-to-colon pH gradient and resistance to mucosa bacterial adhesion. Conversely, oral?+?rectal FMT increased bacterial adhesion, internal organ colonization, and overall mortality. Our results uncovered distinctions in bacterial colonization patterns along the gastrointestinal tract, as well as host tolerability between oral and rectal FMT administration in preterm newborns. Besides, FMT showed the potential to prevent necrotizing enterocolitis.

SUBMITTER: Brunse A

PROVIDER: S-EPMC6461782 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Effect of fecal microbiota transplantation route of administration on gut colonization and host response in preterm pigs.

Brunse Anders A Martin Lena L Rasmussen Torben Sølbeck TS Christensen Lars L Skovsted Cilieborg Malene M Wiese Maria M Khakimov Bekzod B Pieper Robert R Nielsen Dennis Sandris DS Sangild Per Torp PT Thymann Thomas T

The ISME journal 20181026 3

This study examined gut colonization patterns and host responses to fecal microbiota transplantation (FMT) by different administration routes after preterm birth. In two separate experiments, cesarean-delivered, preterm pigs were administered combined oral + rectal, or exclusively rectal donor feces, and compared with saline controls. After 5 days, stomach and colon bacterial compositions were determined by 16S rRNA gene amplicon sequencing, and organic acid metabolites measured. Further, gut pa ...[more]

PMID: 30367124

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Project description:Fecal microbiota transplantation (FMT) can induce clinical remission in ulcerative colitis (UC) patients. Enemas, nasoduodenal tubes, and colonoscopies are the most common routes for FMT administration. However, there is a lack of definitive evidence regarding the effectiveness of capsulized FMT treatment in UC patients. In this study, we administered capsulized FMT to 22 patients with active UC to assess the efficiency of capsulized FMT and determine the specific bacteria and metabolite factors associated with the response to clinical remission. Our results showed that the use of capsulized FMT was successful in the treatment of UC patients. Capsulized FMT induced clinical remission and clinical response in 57.1% (12 of 21) and 76.2% (16 of 21) of UC patients, respectively. Gut bacterial richness was increased after FMT in patients who achieved remission. Patients in remission after FMT exhibited enrichment of Alistipes sp. and Odoribacter splanchnicus, along with increased levels of indolelactic acid. Patients who did not achieve remission exhibited enrichment of Escherichia coli and Klebsiella and increased levels of biosynthesis of 12,13-DiHOME (12,13-dihydroxy-9Z-octadecenoic acid) and lipopolysaccharides. Furthermore, we identified a relationship between specific bacteria and metabolites and the induction of remission in patients. These findings may provide new insights into FMT in UC treatment and provide reference information about therapeutic microbial manipulation of FMT to enhance its effects. (This study has been registered at ClinicalTrails.gov under registration no. NCT03426683). IMPORTANCE Fecal microbiota transplantation has been successfully used in patients. Recently, capsulized FMT was reported to induce a response in patients with UC. However, limited patients were enrolled in such studies, and the functional factors of capsulized FMT have not been reported in the remission of patients with UC. In this study, we prospectively recruited patients with UC to receive capsulized FMT. First, we found that capsulized FMT could induce clinical remission in 57.1% of patients and clinical response in 76.2% after 12 weeks, which was more acceptable. Second, we found a relationship between the decrease of opportunistic pathogen and lipopolysaccharide synthesis in patients in remission after capsulized FMT. We also identified an association between specific bacteria and metabolites and remission induction in patients after capsulized FMT. These findings put forward a possibility for patients to receive FMT at home and provide reference information about therapeutic microbial manipulation of FMT to enhance its effects.

Project description:UnlabelledClostridium difficile infection is one of the most common health care-associated infections, and up to 40% of patients suffer from recurrence of disease following standard antibiotic therapy. Recently, fecal microbiota transplantation (FMT) has been successfully used to treat recurrent C. difficile infection. It is hypothesized that FMT aids in recovery of a microbiota capable of colonization resistance to C. difficile. However, it is not fully understood how this occurs. Here we investigated changes in the fecal microbiota structure following FMT in patients with recurrent C. difficile infection, and imputed a hypothetical functional profile based on the 16S rRNA profile using a predictive metagenomic tool. Increased relative abundance of Bacteroidetes and decreased abundance of Proteobacteria were observed following FMT. The fecal microbiota of recipients following transplantation was more diverse and more similar to the donor profile than the microbiota prior to transplantation. Additionally, we observed differences in the imputed metagenomic profile. In particular, amino acid transport systems were overrepresented in samples collected prior to transplantation. These results suggest that functional changes accompany microbial structural changes following this therapy. Further identification of the specific community members and functions that promote colonization resistance may aid in the development of improved treatment methods for C. difficile infection.ImportanceWithin the last decade, Clostridium difficile infection has surpassed other bacterial infections to become the leading cause of nosocomial infections. Antibiotic use, which disrupts the gut microbiota and its capability in providing colonization resistance against C. difficile, is a known risk factor in C. difficile infection. In particular, recurrent C. difficile remains difficult to treat with standard antibiotic therapy. Fecal microbiota transplantation (FMT) has provided a successful treatment method for some patients with recurrent C. difficile infection, but its mechanism and long-term effects remain unknown. Our results provide insight into the structural and potential metabolic changes that occur following FMT, which may aid in the development of new treatment methods for C. difficile infection.

Project description:The present study was conducted to investigate the effects of early fecal microbiota transplantation on gut development in sucking piglets. A total of 24 3 day-old DLY sucking piglets (2.11 ± 0.15) kg were randomly divided into four groups (TMP, YMP, RMP and control group (CON)), which were transplanted with intact fecal microbiota of Tibetan pig (TP), Yorkshire pig (YP), Rongchang pig (RP), and without transplantation, respectively. The whole trial lasted for 56 d. The results are as follows: when compared with the YMP and RMP treatments, TMP and CON had a lower diarrhea index (P < 0.05), TMP and CON had higher GLP-2 and ANG4 mRNA abundances in the ileum (P < 0.05), and the TMP had a higher jejunal villus height: crypt depth and a higher colonic GLP-2 mRNA abundance (P < 0.05). Moreover, when compared with the YMP and RMP treatments, TMP had an enhanced DMT1 mRNA abundance in the duodenum (P < 0.05), TMP and CON had a greater lactase activity and a higher DMT1 mRNA abundance in the jejunum (P < 0.05), and CON had a higher γ-GT activity in the jejunum (P < 0.05). The jejunal Ca2+, Mg2+-ATPase activity in TMP was higher than that in CON, and the jejunal Na+, K+-ATPase activity in TMP was higher than that in the other three treatments (P < 0.05). Besides, when compared with the YMP and RMP treatments, TMP had a lower MDA content and a higher MUC1 mRNA abundance in the jejunum (P < 0.05); CON had a higher SOD activity in the jejunum (P < 0.05), whereas TMP and CON had a higher butyric acid concentration in the colon and a lower LPS content in the serum (P < 0.05). Finally, when compared with the TMP treatment, the other three treatments had an enhanced IL-10 mRNA abundance in the colon (P < 0.05), YMP and CON had higher counts of Escherichia coli in the colonic digesta (P < 0.05), and the CON had lower counts of Lactobacillus spp in the cecal and colonic digesta (P < 0.05). These data indicated that early transplantation of the fecal microbiota from the Yorkshire pigs and Rongchang pigs to DLY suckling piglets would destroy the gut microbiota balance and thus damage intestinal health.

Dataset Information

Effect of fecal microbiota transplantation route of administration on gut colonization and host response in preterm pigs.

Publications

Effect of fecal microbiota transplantation route of administration on gut colonization and host response in preterm pigs.

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