Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial
ABSTRACTIn small series, third-party fecal microbiota transplantation (FMT) has been successful in decolonizing the gut from clinically relevant antibiotic resistance genes (ARGs). Less is known about the short- and long-term effects of FMT on larger panels of ARGs. We analyzed 226 pre- and post-tre...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2024-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2024.2327442 |
| _version_ | 1827318784425197568 |
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| author | Armin Rashidi Maryam Ebadi Tauseef Ur Rehman Heba Elhusseini David Kazadi Hossam Halaweish Mohammad H. Khan Andrea Hoeschen Qing Cao Xianghua Luo Amanda J. Kabage Sharon Lopez Shernan G. Holtan Daniel J. Weisdorf Chang Liu Satoshi Ishii Alexander Khoruts Christopher Staley |
| author_facet | Armin Rashidi Maryam Ebadi Tauseef Ur Rehman Heba Elhusseini David Kazadi Hossam Halaweish Mohammad H. Khan Andrea Hoeschen Qing Cao Xianghua Luo Amanda J. Kabage Sharon Lopez Shernan G. Holtan Daniel J. Weisdorf Chang Liu Satoshi Ishii Alexander Khoruts Christopher Staley |
| author_sort | Armin Rashidi |
| collection | DOAJ |
| description | ABSTRACTIn small series, third-party fecal microbiota transplantation (FMT) has been successful in decolonizing the gut from clinically relevant antibiotic resistance genes (ARGs). Less is known about the short- and long-term effects of FMT on larger panels of ARGs. We analyzed 226 pre- and post-treatment stool samples from a randomized placebo-controlled trial of FMT in 100 patients undergoing allogeneic hematopoietic cell transplantation or receiving anti-leukemia induction chemotherapy for 47 ARGs. These patients have heavy antibiotic exposure and a high incidence of colonization with multidrug-resistant organisms. Samples from each patient spanned a period of up to 9 months, allowing us to describe both short- and long-term effects of FMT on ARGs, while the randomized design allowed us to distinguish between spontaneous changes vs. FMT effect. We find an overall bimodal pattern. In the first phase (days to weeks after FMT), low-level transfer of ARGs largely associated with commensal healthy donor microbiota occurs. This phase is followed by long-term resistance to new ARGs as stable communities with colonization resistance are formed after FMT. The clinical implications of these findings are likely context-dependent and require further research. In the setting of cancer and intensive therapy, long-term ARG decolonization could translate into fewer downstream infections. |
| first_indexed | 2024-04-25T00:07:37Z |
| format | Article |
| id | doaj.art-044711ae142244d5a2cb20ee21da64fb |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-04-25T00:07:37Z |
| publishDate | 2024-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-044711ae142244d5a2cb20ee21da64fb2024-03-13T17:14:48ZengTaylor & Francis GroupGut Microbes1949-09761949-09842024-12-0116110.1080/19490976.2024.2327442Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trialArmin Rashidi0Maryam Ebadi1Tauseef Ur Rehman2Heba Elhusseini3David Kazadi4Hossam Halaweish5Mohammad H. Khan6Andrea Hoeschen7Qing Cao8Xianghua Luo9Amanda J. Kabage10Sharon Lopez11Shernan G. Holtan12Daniel J. Weisdorf13Chang Liu14Satoshi Ishii15Alexander Khoruts16Christopher Staley17Clinical Research Division, Fred Hutchinson Cancer Center and Division of Oncology, University of Washington, Seattle, WA, USADepartment of Radiation Oncology, University of Washington and Fred Hutchinson Cancer Center, Seattle, WA, USADivision of Hematology, Oncology, and Transplantation, Department of Medicine, University of Minnesota, Minneapolis, MN, USADivision of Hematology, Oncology, and Transplantation, Department of Medicine, University of Minnesota, Minneapolis, MN, USADepartment of Medicine, University of Minnesota, Minneapolis, MN, USADepartment of Surgery, University of Minnesota, Minneapolis, MN, USADepartment of Surgery, University of Minnesota, Minneapolis, MN, USADivision of Hematology, Oncology, and Transplantation, Department of Medicine, University of Minnesota, Minneapolis, MN, USABiostatistics Core, Masonic Cancer Center, University of Minnesota, Minneapolis, MN, USABiostatistics Core, Masonic Cancer Center, University of Minnesota, Minneapolis, MN, USADivision of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, University of Minnesota, Minneapolis, MN, USADivision of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, University of Minnesota, Minneapolis, MN, USADivision of Hematology, Oncology, and Transplantation, Department of Medicine, University of Minnesota, Minneapolis, MN, USADivision of Hematology, Oncology, and Transplantation, Department of Medicine, University of Minnesota, Minneapolis, MN, USADepartment of Soil, Water, and Climate, BioTechnology Institute, University of Minnesota, MN, USADepartment of Soil, Water, and Climate, BioTechnology Institute, University of Minnesota, MN, USADivision of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, University of Minnesota, Minneapolis, MN, USADepartment of Surgery, University of Minnesota, Minneapolis, MN, USAABSTRACTIn small series, third-party fecal microbiota transplantation (FMT) has been successful in decolonizing the gut from clinically relevant antibiotic resistance genes (ARGs). Less is known about the short- and long-term effects of FMT on larger panels of ARGs. We analyzed 226 pre- and post-treatment stool samples from a randomized placebo-controlled trial of FMT in 100 patients undergoing allogeneic hematopoietic cell transplantation or receiving anti-leukemia induction chemotherapy for 47 ARGs. These patients have heavy antibiotic exposure and a high incidence of colonization with multidrug-resistant organisms. Samples from each patient spanned a period of up to 9 months, allowing us to describe both short- and long-term effects of FMT on ARGs, while the randomized design allowed us to distinguish between spontaneous changes vs. FMT effect. We find an overall bimodal pattern. In the first phase (days to weeks after FMT), low-level transfer of ARGs largely associated with commensal healthy donor microbiota occurs. This phase is followed by long-term resistance to new ARGs as stable communities with colonization resistance are formed after FMT. The clinical implications of these findings are likely context-dependent and require further research. In the setting of cancer and intensive therapy, long-term ARG decolonization could translate into fewer downstream infections.https://www.tandfonline.com/doi/10.1080/19490976.2024.2327442Acute myeloid leukemiaantibiotic resistance genefecal microbiota transplantationhematopoietic cell transplantation |
| spellingShingle | Armin Rashidi Maryam Ebadi Tauseef Ur Rehman Heba Elhusseini David Kazadi Hossam Halaweish Mohammad H. Khan Andrea Hoeschen Qing Cao Xianghua Luo Amanda J. Kabage Sharon Lopez Shernan G. Holtan Daniel J. Weisdorf Chang Liu Satoshi Ishii Alexander Khoruts Christopher Staley Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial Gut Microbes Acute myeloid leukemia antibiotic resistance gene fecal microbiota transplantation hematopoietic cell transplantation |
| title | Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial |
| title_full | Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial |
| title_fullStr | Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial |
| title_full_unstemmed | Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial |
| title_short | Long- and short-term effects of fecal microbiota transplantation on antibiotic resistance genes: results from a randomized placebo-controlled trial |
| title_sort | long and short term effects of fecal microbiota transplantation on antibiotic resistance genes results from a randomized placebo controlled trial |
| topic | Acute myeloid leukemia antibiotic resistance gene fecal microbiota transplantation hematopoietic cell transplantation |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2024.2327442 |
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