Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases

Fecal microbiota transplantation (FMT), which is thought to have the potential to correct dysbiosis of gut microbiota, has been used to treat inflammatory bowel disease (IBD) for almost a decade. Here, we report an interventional prospective cohort study performed to elucidate the extent of and proc...

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Main Authors: Manli Zou, Zhuye Jie, Bota Cui, Honggang Wang, Qiang Feng, Yuanqiang Zou, Xiuqing Zhang, Huanming Yang, Jian Wang, Faming Zhang, Huijue Jia
Format: Article
Language:English
Published: Wiley 2020-01-01
Series:FEBS Open Bio
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Online Access:https://doi.org/10.1002/2211-5463.12744
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author Manli Zou
Zhuye Jie
Bota Cui
Honggang Wang
Qiang Feng
Yuanqiang Zou
Xiuqing Zhang
Huanming Yang
Jian Wang
Faming Zhang
Huijue Jia
author_facet Manli Zou
Zhuye Jie
Bota Cui
Honggang Wang
Qiang Feng
Yuanqiang Zou
Xiuqing Zhang
Huanming Yang
Jian Wang
Faming Zhang
Huijue Jia
author_sort Manli Zou
collection DOAJ
description Fecal microbiota transplantation (FMT), which is thought to have the potential to correct dysbiosis of gut microbiota, has been used to treat inflammatory bowel disease (IBD) for almost a decade. Here, we report an interventional prospective cohort study performed to elucidate the extent of and processes underlying microbiota engraftment in IBD patients after FMT treatment. The cohort included two categories of patients: (a) patients with moderate to severe Crohn’s disease (CD) (Harvey–Bradshaw Index ≥ 7, n = 11) and (b) patients with ulcerative colitis (UC) (Montreal classification S2 and S3, n = 4). All patients were treated with a single FMT (via mid‐gut, from healthy donors), and follow‐up visits were performed at baseline, 3 days, 1 week, and 1 month after FMT (missing time points included). At each follow‐up time point, fecal samples and clinical metadata were collected. For comparative analysis, 10 fecal samples from 10 healthy donors were included to represent the diversity level of normal gut microbiota. Additionally, the metagenomic data of 25 fecal samples from five individuals with metabolic syndrome who underwent autologous FMT treatment were downloaded from a previous published paper to represent fluctuations in microbiota induced during FMT. All fecal samples underwent shotgun metagenomic sequencing. We found that 3 days after FMT, 11 out of 15 recipients were in remission (three out of four UC recipients; 8 out of 11 CD recipients). Generally, bacterial colonization was observed to be lower in CD recipients than in UC recipients at both species and strain levels. Furthermore, across species, different strains displayed disease‐specific displacement advantages under two‐disease status. Finally, most post‐FMT species (> 80%) could be properly predicted (area under the curve > 85%) using a random forest classification model, with the gut microbiota composition and clinical parameters of pre‐FMT recipients acting as factors that contribute to prediction accuracy.
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spelling doaj-art-f68c57b61be14d3c8656a1a972d83b452024-12-09T14:15:33ZengWileyFEBS Open Bio2211-54632020-01-01101415510.1002/2211-5463.12744Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseasesManli Zou0Zhuye Jie1Bota Cui2Honggang Wang3Qiang Feng4Yuanqiang Zou5Xiuqing Zhang6Huanming Yang7Jian Wang8Faming Zhang9Huijue Jia10BGI Education Center University of Chinese Academy of Sciences Shenzhen ChinaBGI‐Shenzhen ChinaMedical Center for Digestive Disease the Second Affiliated Hospital of Nanjing Medical University ChinaMedical Center for Digestive Disease the Second Affiliated Hospital of Nanjing Medical University ChinaBGI‐Shenzhen ChinaBGI‐Shenzhen ChinaBGI Education Center University of Chinese Academy of Sciences Shenzhen ChinaBGI‐Shenzhen ChinaBGI‐Shenzhen ChinaMedical Center for Digestive Disease the Second Affiliated Hospital of Nanjing Medical University ChinaBGI‐Shenzhen ChinaFecal microbiota transplantation (FMT), which is thought to have the potential to correct dysbiosis of gut microbiota, has been used to treat inflammatory bowel disease (IBD) for almost a decade. Here, we report an interventional prospective cohort study performed to elucidate the extent of and processes underlying microbiota engraftment in IBD patients after FMT treatment. The cohort included two categories of patients: (a) patients with moderate to severe Crohn’s disease (CD) (Harvey–Bradshaw Index ≥ 7, n = 11) and (b) patients with ulcerative colitis (UC) (Montreal classification S2 and S3, n = 4). All patients were treated with a single FMT (via mid‐gut, from healthy donors), and follow‐up visits were performed at baseline, 3 days, 1 week, and 1 month after FMT (missing time points included). At each follow‐up time point, fecal samples and clinical metadata were collected. For comparative analysis, 10 fecal samples from 10 healthy donors were included to represent the diversity level of normal gut microbiota. Additionally, the metagenomic data of 25 fecal samples from five individuals with metabolic syndrome who underwent autologous FMT treatment were downloaded from a previous published paper to represent fluctuations in microbiota induced during FMT. All fecal samples underwent shotgun metagenomic sequencing. We found that 3 days after FMT, 11 out of 15 recipients were in remission (three out of four UC recipients; 8 out of 11 CD recipients). Generally, bacterial colonization was observed to be lower in CD recipients than in UC recipients at both species and strain levels. Furthermore, across species, different strains displayed disease‐specific displacement advantages under two‐disease status. Finally, most post‐FMT species (> 80%) could be properly predicted (area under the curve > 85%) using a random forest classification model, with the gut microbiota composition and clinical parameters of pre‐FMT recipients acting as factors that contribute to prediction accuracy.https://doi.org/10.1002/2211-5463.12744fecal microbiota transplantationinflammatory bowel diseaserandom forestshotgun metagenomic sequencingstrain displacementstrain‐level identification
spellingShingle Manli Zou
Zhuye Jie
Bota Cui
Honggang Wang
Qiang Feng
Yuanqiang Zou
Xiuqing Zhang
Huanming Yang
Jian Wang
Faming Zhang
Huijue Jia
Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
FEBS Open Bio
fecal microbiota transplantation
inflammatory bowel disease
random forest
shotgun metagenomic sequencing
strain displacement
strain‐level identification
title Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
title_full Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
title_fullStr Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
title_full_unstemmed Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
title_short Fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
title_sort fecal microbiota transplantation results in bacterial strain displacement in patients with inflammatory bowel diseases
topic fecal microbiota transplantation
inflammatory bowel disease
random forest
shotgun metagenomic sequencing
strain displacement
strain‐level identification
url https://doi.org/10.1002/2211-5463.12744
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