A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process
ABSTRACT Fecal microbiota transplantation (FMT) targeting gut microbiota has recently been applied to the treatment of ulcerative colitis (UC). However, preliminary trials showed that only a subset of patients responded to FMT, and the heterogeneity in donor gut microbiota probably played important...
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| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02159-21 |
| _version_ | 1828033545821487104 |
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| author | Bangzhou Zhang Luxi Yang Hanbing Ning Man Cao Zhangran Chen Qiongyun Chen Guanghui Lian Hailing Tang Qizhi Wang Junping Wang Zhihui Lin Jianbo Wen Yuedong Liu Ji Xuan Xuejun Li Aiqiang Lin Jianquan He Lei Zhang Xiaohua Hou Qiang Zeng Chuanxing Xiao |
| author_facet | Bangzhou Zhang Luxi Yang Hanbing Ning Man Cao Zhangran Chen Qiongyun Chen Guanghui Lian Hailing Tang Qizhi Wang Junping Wang Zhihui Lin Jianbo Wen Yuedong Liu Ji Xuan Xuejun Li Aiqiang Lin Jianquan He Lei Zhang Xiaohua Hou Qiang Zeng Chuanxing Xiao |
| author_sort | Bangzhou Zhang |
| collection | DOAJ |
| description | ABSTRACT Fecal microbiota transplantation (FMT) targeting gut microbiota has recently been applied to the treatment of ulcerative colitis (UC). However, preliminary trials showed that only a subset of patients responded to FMT, and the heterogeneity in donor gut microbiota probably played important roles in patients’ responses, implying the significance of matching an appropriate donor to a specified patient. We developed a strategy to build a donor-recipient matching model to guide rational donor selection for UC in FMT. We collected and uniformly reanalyzed 656 fecal 16S rRNA gene sequencing samples (350 from UC patients and 306 from healthy subjects) from 9 studies. Significantly lower α-diversity indexes were observed in UC patients by random effects model. Thirty-four bacterial genera and 34 predicted pathways were identified with significant odds ratios and classification potentials for UC patients. Based on six bacterial indicators, including richness, overall distance, genera, and pathways (beneficial and harmful), the analytic hierarchy process-based donor-recipient matching model was set to rank and select appropriate donors for patients with UC. Finally, the model showed favorable classification powers (>70%) for FMT effectiveness in two previous clinical trials. This study revealed the dysbiosis of fecal bacterial diversity, composition, and predicted pathways of patients with UC by meta-analysis and hereby developed a donor-recipient matching strategy to guide donor selection for UC in FMT. This strategy can also be applied to other diseases associated with gut microbiota. IMPORTANCE Modulation of gut microbiota by FMT from donors has been applied to the treatment of UC and yielded variable effectiveness in clinical trials. One possibility is that this variable effectiveness was related to donor selection, as a patient’s response to FMT may rely on the capability of the used donor’s microbiota to restore the specific gut disturbances of the patient. However, the biggest issues on the practical level are what should be considered in the selection process and how to set up such a donor-recipient matching model. In this study, we presented a bacterial profile-based donor-recipient matching strategy to guide donor selection for UC in FMT by first meta-analysis of 656 fecal 16S rRNA gene sequencing samples from 9 studies to identify significant indicators and then setting up the model by an analytic hierarchy process. The applicability and accuracy of this model were verified in the data sets from two previous FMT clinical studies. Our data indicate that the donor-recipient matching model built in this study enables researchers to rationally select donors for UC patients in FMT clinical practice, although it needs more samples and prospective trials for validation. The strategy adopted in this study to leverage existing data sets to build donor-recipient matching models for precision FMT is feasible for other diseases associated with gut microbiota. |
| first_indexed | 2024-04-10T15:21:14Z |
| format | Article |
| id | doaj.art-213ec02c3efa456cb95ee4f0ab8eef70 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-10T15:21:14Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-213ec02c3efa456cb95ee4f0ab8eef702023-02-14T14:15:49ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.02159-21A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy ProcessBangzhou Zhang0Luxi Yang1Hanbing Ning2Man Cao3Zhangran Chen4Qiongyun Chen5Guanghui Lian6Hailing Tang7Qizhi Wang8Junping Wang9Zhihui Lin10Jianbo Wen11Yuedong Liu12Ji Xuan13Xuejun Li14Aiqiang Lin15Jianquan He16Lei Zhang17Xiaohua Hou18Qiang Zeng19Chuanxing Xiao20School of Life Sciences, Xiamen University, Xiamen, ChinaSchool of Life Sciences, Xiamen University, Xiamen, ChinaDepartment of Digestive Diseases, First Affiliated Hospital of Zhengzhou University, Zhengzhou, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen, ChinaSchool of Medicine, Xiamen University, Xiamen, ChinaSchool of Medicine, Xiamen University, Xiamen, ChinaDepartment of Gastroenterology, Xiangya Hospital, Changsha, ChinaDepartment of Gastroenterology, Xi'an Central Hospital, Xi’an, ChinaDepartment of Gastroenterology, The First Affiliated Hospital of Bengbu Medical College, Bengbu, ChinaDepartment of Gastroenterology, The Affiliated People's Hospital of Shanxi Medical University, Taiyuan, Shanxi, ChinaDepartment of Gastroenterology, Fujian Provincial Hospital, Fuzhou, ChinaDepartment of Gastroenterology, Pingxiang People’s Hospital, Pingxiang, ChinaDepartment of Gastroenterology, The Third Affiliated Hospital of Liaoning University of Traditional Chinese Medicine, Shenyang, ChinaDepartment of Gastroenterology, Jinling Hospital, Nanjing, ChinaDepartment of Gastroenterology, The Second Affiliated Hospital of Anhui University of Traditional Chinese Medicine, Hefei, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen, ChinaSchool of Medicine, Xiamen University, Xiamen, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Technology and Science, Wuhan, ChinaDivision of Gastroenterology, Union Hospital, Tongji Medical College, Huazhong University of Technology and Science, Wuhan, ChinaHealth Management Institute, The Second Medical Center & National Clinical Research Center for Geriatric Diseases, Chinese PLA General Hospital, Beijing, ChinaXiamen Treatgut Biotechnology Co., Ltd., Xiamen, ChinaABSTRACT Fecal microbiota transplantation (FMT) targeting gut microbiota has recently been applied to the treatment of ulcerative colitis (UC). However, preliminary trials showed that only a subset of patients responded to FMT, and the heterogeneity in donor gut microbiota probably played important roles in patients’ responses, implying the significance of matching an appropriate donor to a specified patient. We developed a strategy to build a donor-recipient matching model to guide rational donor selection for UC in FMT. We collected and uniformly reanalyzed 656 fecal 16S rRNA gene sequencing samples (350 from UC patients and 306 from healthy subjects) from 9 studies. Significantly lower α-diversity indexes were observed in UC patients by random effects model. Thirty-four bacterial genera and 34 predicted pathways were identified with significant odds ratios and classification potentials for UC patients. Based on six bacterial indicators, including richness, overall distance, genera, and pathways (beneficial and harmful), the analytic hierarchy process-based donor-recipient matching model was set to rank and select appropriate donors for patients with UC. Finally, the model showed favorable classification powers (>70%) for FMT effectiveness in two previous clinical trials. This study revealed the dysbiosis of fecal bacterial diversity, composition, and predicted pathways of patients with UC by meta-analysis and hereby developed a donor-recipient matching strategy to guide donor selection for UC in FMT. This strategy can also be applied to other diseases associated with gut microbiota. IMPORTANCE Modulation of gut microbiota by FMT from donors has been applied to the treatment of UC and yielded variable effectiveness in clinical trials. One possibility is that this variable effectiveness was related to donor selection, as a patient’s response to FMT may rely on the capability of the used donor’s microbiota to restore the specific gut disturbances of the patient. However, the biggest issues on the practical level are what should be considered in the selection process and how to set up such a donor-recipient matching model. In this study, we presented a bacterial profile-based donor-recipient matching strategy to guide donor selection for UC in FMT by first meta-analysis of 656 fecal 16S rRNA gene sequencing samples from 9 studies to identify significant indicators and then setting up the model by an analytic hierarchy process. The applicability and accuracy of this model were verified in the data sets from two previous FMT clinical studies. Our data indicate that the donor-recipient matching model built in this study enables researchers to rationally select donors for UC patients in FMT clinical practice, although it needs more samples and prospective trials for validation. The strategy adopted in this study to leverage existing data sets to build donor-recipient matching models for precision FMT is feasible for other diseases associated with gut microbiota.https://journals.asm.org/doi/10.1128/spectrum.02159-2116S rRNA gene sequencingmeta-analysisanalytic hierarchy processdonor-recipient matchingulcerative colitisfecal microbiota transplantation |
| spellingShingle | Bangzhou Zhang Luxi Yang Hanbing Ning Man Cao Zhangran Chen Qiongyun Chen Guanghui Lian Hailing Tang Qizhi Wang Junping Wang Zhihui Lin Jianbo Wen Yuedong Liu Ji Xuan Xuejun Li Aiqiang Lin Jianquan He Lei Zhang Xiaohua Hou Qiang Zeng Chuanxing Xiao A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process Microbiology Spectrum 16S rRNA gene sequencing meta-analysis analytic hierarchy process donor-recipient matching ulcerative colitis fecal microbiota transplantation |
| title | A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process |
| title_full | A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process |
| title_fullStr | A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process |
| title_full_unstemmed | A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process |
| title_short | A Matching Strategy To Guide Donor Selection for Ulcerative Colitis in Fecal Microbiota Transplantation: Meta-Analysis and Analytic Hierarchy Process |
| title_sort | matching strategy to guide donor selection for ulcerative colitis in fecal microbiota transplantation meta analysis and analytic hierarchy process |
| topic | 16S rRNA gene sequencing meta-analysis analytic hierarchy process donor-recipient matching ulcerative colitis fecal microbiota transplantation |
| url | https://journals.asm.org/doi/10.1128/spectrum.02159-21 |
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