Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection

Abstract Background Alteration of the gut microbiota by repeated antibiotic treatment increases susceptibility to Clostridioides difficile infection. Faecal microbiota transplantation from donors with a normal microbiota effectively treats C. difficile infection. Methods The study involved 10 patien...

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Main Authors: Jillian R.-M. Brown, Burkhardt Flemer, Susan A. Joyce, Akbar Zulquernain, Donal Sheehan, Fergus Shanahan, Paul W. O’Toole
Format: Article
Language:English
Published: BMC 2018-08-01
Series:BMC Gastroenterology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12876-018-0860-5
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author Jillian R.-M. Brown
Burkhardt Flemer
Susan A. Joyce
Akbar Zulquernain
Donal Sheehan
Fergus Shanahan
Paul W. O’Toole
author_facet Jillian R.-M. Brown
Burkhardt Flemer
Susan A. Joyce
Akbar Zulquernain
Donal Sheehan
Fergus Shanahan
Paul W. O’Toole
author_sort Jillian R.-M. Brown
collection DOAJ
description Abstract Background Alteration of the gut microbiota by repeated antibiotic treatment increases susceptibility to Clostridioides difficile infection. Faecal microbiota transplantation from donors with a normal microbiota effectively treats C. difficile infection. Methods The study involved 10 patients with recurrent C. difficile infection, nine of whom received transplants from individual donors and one who received a donor unit from a stool bank (OpenBiome). Results All individuals demonstrated enduring post-transplant resolution of C. difficile- associated diarrhoea. Faecal microbiota diversity of recipients significantly increased, and the composition of the microbiota resembled that of the donor. Patients with C. difficile infection exhibited significantly lower faecal levels of secondary/ bile acids and higher levels of primary bile acids. Levels of secondary bile acids were restored in all transplant recipients, but to a lower degree with the OpenBiome transplant. The abundance increased of bacterial genera known from previous studies to confer resistance to growth and germination of C. difficile. These were significantly negatively associated with primary bile acid levels and positively related with secondary bile acid levels. Although reduced levels of the short chain fatty acids, butyrate, propionate and acetate, have been previously reported, here we report elevations in SCFA, pyruvic and lactic fatty acids, saturated, ω-6, monounsaturated, ω-3 and ω-6 polyunsaturated fatty acids (PUFA) in C. difficile infection. This potentially indicates one or a combination of increased dietary FA intake, microbial modification of FAs or epithelial cell damage and inflammatory cell recruitment. No reversion to donor FA profile occurred post-FMT but ω-3 to ω-6 PUFA ratios were altered in the direction of the donor. Archaeal metabolism genes were found in some samples post FMT. Conclusion A consistent metabolic signature was identified in the post-transplant microbiota, with reduced primary bile acids and substantial restoration of secondary bile acid production capacity. Total FA levels were unchanged but the ratio of inflammatory to non-inflammatory FAs decreased.
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spelling doaj.art-1689773be7eb4c80aba556635bbf18112022-12-21T23:51:38ZengBMCBMC Gastroenterology1471-230X2018-08-0118111510.1186/s12876-018-0860-5Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infectionJillian R.-M. Brown0Burkhardt Flemer1Susan A. Joyce2Akbar Zulquernain3Donal Sheehan4Fergus Shanahan5Paul W. O’Toole6APC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAPC Microbiome Institute, University College Cork, National University of IrelandAbstract Background Alteration of the gut microbiota by repeated antibiotic treatment increases susceptibility to Clostridioides difficile infection. Faecal microbiota transplantation from donors with a normal microbiota effectively treats C. difficile infection. Methods The study involved 10 patients with recurrent C. difficile infection, nine of whom received transplants from individual donors and one who received a donor unit from a stool bank (OpenBiome). Results All individuals demonstrated enduring post-transplant resolution of C. difficile- associated diarrhoea. Faecal microbiota diversity of recipients significantly increased, and the composition of the microbiota resembled that of the donor. Patients with C. difficile infection exhibited significantly lower faecal levels of secondary/ bile acids and higher levels of primary bile acids. Levels of secondary bile acids were restored in all transplant recipients, but to a lower degree with the OpenBiome transplant. The abundance increased of bacterial genera known from previous studies to confer resistance to growth and germination of C. difficile. These were significantly negatively associated with primary bile acid levels and positively related with secondary bile acid levels. Although reduced levels of the short chain fatty acids, butyrate, propionate and acetate, have been previously reported, here we report elevations in SCFA, pyruvic and lactic fatty acids, saturated, ω-6, monounsaturated, ω-3 and ω-6 polyunsaturated fatty acids (PUFA) in C. difficile infection. This potentially indicates one or a combination of increased dietary FA intake, microbial modification of FAs or epithelial cell damage and inflammatory cell recruitment. No reversion to donor FA profile occurred post-FMT but ω-3 to ω-6 PUFA ratios were altered in the direction of the donor. Archaeal metabolism genes were found in some samples post FMT. Conclusion A consistent metabolic signature was identified in the post-transplant microbiota, with reduced primary bile acids and substantial restoration of secondary bile acid production capacity. Total FA levels were unchanged but the ratio of inflammatory to non-inflammatory FAs decreased.http://link.springer.com/article/10.1186/s12876-018-0860-5Clostridioides difficileFaecal microbiota transplantationBile acidsFatty acidsArchaea
spellingShingle Jillian R.-M. Brown
Burkhardt Flemer
Susan A. Joyce
Akbar Zulquernain
Donal Sheehan
Fergus Shanahan
Paul W. O’Toole
Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
BMC Gastroenterology
Clostridioides difficile
Faecal microbiota transplantation
Bile acids
Fatty acids
Archaea
title Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
title_full Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
title_fullStr Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
title_full_unstemmed Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
title_short Changes in microbiota composition, bile and fatty acid metabolism, in successful faecal microbiota transplantation for Clostridioides difficile infection
title_sort changes in microbiota composition bile and fatty acid metabolism in successful faecal microbiota transplantation for clostridioides difficile infection
topic Clostridioides difficile
Faecal microbiota transplantation
Bile acids
Fatty acids
Archaea
url http://link.springer.com/article/10.1186/s12876-018-0860-5
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