Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes

Fecal microbiota transplantation (FMT) is under investigation for several indications, including ulcerative colitis (UC). The clinical success of FMT depends partly on the engraftment of viable bacteria. Because the vast majority of human gut microbiota consists of anaerobes, the currently used aero...

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Main Authors: Mèlanie V. Bénard, Iñaki Arretxe, Koen Wortelboer, Hermie J. M. Harmsen, Mark Davids, Clara M. A. de Bruijn, Marc A. Benninga, Floor Hugenholtz, Hilde Herrema, Cyriel Y. Ponsioen
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/9/2238
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author Mèlanie V. Bénard
Iñaki Arretxe
Koen Wortelboer
Hermie J. M. Harmsen
Mark Davids
Clara M. A. de Bruijn
Marc A. Benninga
Floor Hugenholtz
Hilde Herrema
Cyriel Y. Ponsioen
author_facet Mèlanie V. Bénard
Iñaki Arretxe
Koen Wortelboer
Hermie J. M. Harmsen
Mark Davids
Clara M. A. de Bruijn
Marc A. Benninga
Floor Hugenholtz
Hilde Herrema
Cyriel Y. Ponsioen
author_sort Mèlanie V. Bénard
collection DOAJ
description Fecal microbiota transplantation (FMT) is under investigation for several indications, including ulcerative colitis (UC). The clinical success of FMT depends partly on the engraftment of viable bacteria. Because the vast majority of human gut microbiota consists of anaerobes, the currently used aerobic processing protocols of donor stool may diminish the bacterial viability of transplanted material. This study assessed the effect of four processing techniques for donor stool (i.e., anaerobic and aerobic, both direct processing and after temporary cool storage) on bacterial viability. By combining anaerobic culturing on customized media for anaerobes with 16S rRNA sequencing, we could successfully culture and identify the majority of the bacteria present in raw fecal suspensions. We show that direct anaerobic processing of donor stool is superior to aerobic processing conditions for preserving the bacterial viability of obligate anaerobes and butyrate-producing bacteria related to the clinical response to FMT in ulcerative colitis patients, including <i>Faecalibacterium</i>, <i>Eubacterium hallii</i>, and <i>Blautia</i>. The effect of oxygen exposure during stool processing decreased when the samples were stored long-term. Our results confirm the importance of sample conditioning to preserve the bacterial viability of oxygen-sensitive gut bacteria. Anaerobic processing of donor stool may lead to increased clinical success of FMT, which should further be investigated in clinical trials.
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spelling doaj.art-a30de248f75e4d489c38dd78c03a596f2023-11-19T12:02:32ZengMDPI AGMicroorganisms2076-26072023-09-01119223810.3390/microorganisms11092238Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate AnaerobesMèlanie V. Bénard0Iñaki Arretxe1Koen Wortelboer2Hermie J. M. Harmsen3Mark Davids4Clara M. A. de Bruijn5Marc A. Benninga6Floor Hugenholtz7Hilde Herrema8Cyriel Y. Ponsioen9Department of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Experimental Vascular Medicine, Amsterdam Cardiovascular Sciences (ACS), Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Medical Microbiology and Infection Prevention, University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The NetherlandsDepartment of Experimental Vascular Medicine, Amsterdam Cardiovascular Sciences (ACS), Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsCenter for Experimental and Molecular Medicine, Amsterdam Medical Center, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Experimental Vascular Medicine, Amsterdam Cardiovascular Sciences (ACS), Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsDepartment of Gastroenterology and Hepatology, Amsterdam Gastroenterology Endocrinology Metabolism (AGEM), Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, The NetherlandsFecal microbiota transplantation (FMT) is under investigation for several indications, including ulcerative colitis (UC). The clinical success of FMT depends partly on the engraftment of viable bacteria. Because the vast majority of human gut microbiota consists of anaerobes, the currently used aerobic processing protocols of donor stool may diminish the bacterial viability of transplanted material. This study assessed the effect of four processing techniques for donor stool (i.e., anaerobic and aerobic, both direct processing and after temporary cool storage) on bacterial viability. By combining anaerobic culturing on customized media for anaerobes with 16S rRNA sequencing, we could successfully culture and identify the majority of the bacteria present in raw fecal suspensions. We show that direct anaerobic processing of donor stool is superior to aerobic processing conditions for preserving the bacterial viability of obligate anaerobes and butyrate-producing bacteria related to the clinical response to FMT in ulcerative colitis patients, including <i>Faecalibacterium</i>, <i>Eubacterium hallii</i>, and <i>Blautia</i>. The effect of oxygen exposure during stool processing decreased when the samples were stored long-term. Our results confirm the importance of sample conditioning to preserve the bacterial viability of oxygen-sensitive gut bacteria. Anaerobic processing of donor stool may lead to increased clinical success of FMT, which should further be investigated in clinical trials.https://www.mdpi.com/2076-2607/11/9/2238fecal microbiota transplantationculturabilitybacterial viabilitygut microbiotaulcerative colitisanaerobic bacteria
spellingShingle Mèlanie V. Bénard
Iñaki Arretxe
Koen Wortelboer
Hermie J. M. Harmsen
Mark Davids
Clara M. A. de Bruijn
Marc A. Benninga
Floor Hugenholtz
Hilde Herrema
Cyriel Y. Ponsioen
Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
Microorganisms
fecal microbiota transplantation
culturability
bacterial viability
gut microbiota
ulcerative colitis
anaerobic bacteria
title Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
title_full Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
title_fullStr Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
title_full_unstemmed Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
title_short Anaerobic Feces Processing for Fecal Microbiota Transplantation Improves Viability of Obligate Anaerobes
title_sort anaerobic feces processing for fecal microbiota transplantation improves viability of obligate anaerobes
topic fecal microbiota transplantation
culturability
bacterial viability
gut microbiota
ulcerative colitis
anaerobic bacteria
url https://www.mdpi.com/2076-2607/11/9/2238
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