Faecal microbiota transplantation for Clostridioides difficile: mechanisms and pharmacology

Khoruts, Alexander; Staley, Christopher; Sadowsky, Michael J.

doi:10.1038/s41575-020-0350-4

Cited by 158Clostridium difficile and Clostridium perfringens researchGut microbiota and healthGastrointestinal motility and disorders

Faecal microbiota transplantation for Clostridioides difficile: mechanisms and pharmacology

Khoruts, Alexander, Staley, Christopher, Sadowsky, Michael J.·2021·Nature Reviews Gastroenterology & Hepatology

DOI 10.1038/s41575-020-0350-4

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Abstract

Faecal microbiota transplantation (FMT) has emerged as a remarkably successful treatment for recurrent Clostridioides difficile infection that cannot be cured with antibiotics alone. Understanding the complex biology and pathogenesis of C. difficile infection, which we discuss in this Perspective, is essential for understanding the potential mechanisms by which FMT cures this disease. Although FMT has already entered clinical practice, different microbiota-based products are currently in clinical trials and are vying for regulatory approval. However, all these therapeutics belong to an entirely new class of agents that require the development of a new branch of pharmacology. Characterization of microbiota therapeutics uses novel and rapidly evolving technologies and requires incorporation of microbial ecology concepts. Here, we consider FMT within a pharmacological framework, including its essential elements: formulation, pharmacokinetics and pharmacodynamics. From this viewpoint, multiple gaps in knowledge become apparent, identifying areas that require systematic research. This knowledge is needed to help clinical providers use microbiota therapeutics appropriately and to facilitate development of next-generation microbiota products with improved safety and efficacy. The discussion here is limited to FMT as a representative of microbiota therapeutics and recurrent C. difficile as the indication; however, consideration of the intrinsic basic principles is relevant to this entire class of microbiota-based therapeutics.

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FMT has undergone significant advancements over the years, evolving from a relatively crude procedure of transferring fresh donor stool to a mainstream treatment option.
“However, FMT has undergone significant advancements over the years, evolving from a relatively crude procedure of transferring fresh donor stool to a mainstream treatment option.”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [727]
The evolution of FMT is enabled by the development of standardized FMT products, with increased emphasis on their pharmaceutical formulation, pharmacokinetics, pharmacodynamics, and toxicity.
“This evolution is enabled by the development of standardized FMT products, with increased emphasis on their pharmaceutical formulation, pharmacokinetics, pharmacodynamics, and toxicity.727”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [727]

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The Antibacterial Lectin RegIII-Gamma Promotes the Spatial Segregation of Microbiota and Host in the Intestine
Gern, J. E. (2012) · PEDIATRICS · doi:10.1542/peds.2012-2183bbbb · Cited by 56 · see citing works
Comparison of Different Strategies for Providing Fecal Microbiota Transplantation to Treat Patients with Recurrent Clostridium difficile Infection in Two English Hospitals: A Review
Goldenberg, S. D., Batra, R., Beales, I., Digby-Bell, J. L., Irving, P. M., Kellingray, L., Narbad, A., & Elumogo, N. (2018) · Infectious Diseases and Therapy · doi:10.1007/s40121-018-0189-y · Cited by 56 · see citing works
Development of Fecal Microbiota Transplantation Suitable for Mainstream Medicine
Khoruts, A., Sadowsky, M. J., & Hamilton, M. J. (2014) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2014.11.014 · Cited by 55 · see citing works
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Community dynamics drive punctuated engraftment of the fecal microbiome following transplantation using freeze-dried, encapsulated fecal microbiota
Staley, C. M., Vaughn, B. P., Graiziger, C. T., Singroy, S., Hamilton, M. J., Yao, D., Chen, C., Khoruts, A., & Sadowsky, M. J. (2017) · Gut Microbes · doi:10.1080/19490976.2017.1299310 · Cited by 55 · see citing works
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How Patients View Probiotics
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On the Survival of Frozen Bacteria
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Humoral immune response as predictor of recurrence in Clostridium difficile infection
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Improving regulation of microbiota transplants
Hoffmann, D. E., Palumbo, F. B., Ravel, J., Roghmann, M., Rowthorn, V., & von Rosenvinge, E. C. (2017) · Science · doi:10.1126/science.aaq0034 · Cited by 52 · see citing works
Human Transmission of Blastocystis by Fecal Microbiota Transplantation Without Development of Gastrointestinal Symptoms in Recipients
Terveer, E. M., van Gool, T., Ooijevaar, R. E., Sanders, I. M. J. G., Boeije‐Koppenol, E., Keller, J. J., Bart, A., Kuijper, E. J., Netherlands Donor Feces Bank (NDFB) Study Group, Terveer, E. M., et al. (2019) · Clinical Infectious Diseases · doi:10.1093/cid/ciz1122 · Cited by 51 · see citing works
The success of fecal microbial transplantation in Clostridium difficile infection correlates with bacteriophage relative abundance in the donor: a retrospective cohort study
Park, H., Laffin, M., Jovel, J., Millan, B., Hyun, J. E., Hotte, N., Kao, D. H., & Madsen, K. L. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1586037 · Cited by 49 · see citing works
Mechanisms of hypervirulent Clostridium difficile ribotype 027 displacement of endemic strains: an epidemiological model
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BaiCD gene cluster abundance is negatively correlated with Clostridium difficile infection
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Long‐term microbiota and virome in a Zürich patient after fecal transplantation against Clostridium difficile infection
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Microbiota transplant therapy and autism: lessons for the clinic
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Environmental Contamination in Households of Patients with Recurrent Clostridium difficile Infection
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The Mycobiome: Influencing IBD Severity
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Helicobacter pylori and Clostridium difficile in Cystic Fibrosis Patients
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Increased Risk of Functional Gastrointestinal Sequelae After Clostridium difficile Infection Among Active Duty United States Military Personnel (1998–2010)
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Vancomycin Treatment Alters Humoral Immunity and Intestinal Microbiota in an Aged Mouse Model ofClostridium difficileInfection
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Real-Time Cellular Analysis Coupled with a Specimen Enrichment Accurately Detects and Quantifies Clostridium difficile Toxins in Stool
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Adaptive immune response to Clostridium difficile infection: A perspective for prevention and therapy
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EVIDENCE OF CYTOPLASMIC MEMBRANE INJURY IN THE DRYING OF BACTERIA
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Cephamycins inhibit pathogen sporulation and effectively treat recurrent Clostridioides difficile infection
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Classifying Fecal Microbiota Transplantation Failure: An Observational Study Examining Timing and Characteristics of Fecal Microbiota Transplantation Failures
Allegretti, J. R., Allegretti, A. S., Phelps, E. L., Xu, H., Fischer, M., & Kassam, Z. (2017) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2017.10.031 · Cited by 32 · see citing works
Clostridium difficile fecal toxin level is associated with disease severity and prognosis
Cohen, N. A., Miller, T., Na’aminh, W., Hod, K., Adler, A., Cohen, D., Guzner‐Gur, H., Santo, E., Halpern, Z., Carmeli, Y., et al. (2017) · United European Gastroenterology Journal · doi:10.1177/2050640617750809 · Cited by 32 · see citing works
Risk of Clostridium difficile Infection with Systemic Antimicrobial Therapy Following Successful Fecal Microbiota Transplant: Should We Recommend Anti-Clostridium difficile Antibiotic Prophylaxis?
Allegretti, J. R., Kao, D. H., Phelps, E. L., Roach, B., Smith, J. D., Ganapini, V., Kassam, Z., Xu, H., & Fischer, M. (2019) · Digestive Diseases and Sciences · doi:10.1007/s10620-018-5450-4 · Cited by 30 · see citing works
The Impact of Regulatory Policies on the Future of Fecal Microbiota Transplantation
Khoruts, A., Hoffmann, D. E., & Palumbo, F. B. (2019) · The Journal of Law Medicine & Ethics · doi:10.1177/1073110519897726 · Cited by 26 · see citing works
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Preservation of Microorganisms by Freeze-drying
BENEDICT, R. G., Sharpe, E. S., Corman, J., Meyers, G. B., Baer, E. F., HALL, H. H., & Jackson, R. W. (1961) · Applied Microbiology · doi:10.1128/aem.9.3.256-262.1961 · Cited by 25 · see citing works
Banking feces: a new frontier for public blood banks?
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Do the Microbiota Influence Vaccines and Protective Immunity to Pathogens?Preprint
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PURLs: prescribing an antibiotic? Pair it with probiotics.
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A simple and inexpensive enteric-coated capsule for delivery of acid-labile macromolecules to the small intestine
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Preservation of Microorganisms by Freeze-Drying
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Fecal Microbiota Transplant: A Rose by Any Other Name
Khoruts, A., & Brandt, L. J. (2019) · The American Journal of Gastroenterology · doi:10.14309/ajg.0000000000000286 · Cited by 18 · see citing works
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Decreased Complexity of Serum N-glycan Structures Associates with Successful Fecal Microbiota Transplantation for Recurrent Clostridioides difficile Infection
Monaghan, T. M., Pučić‐Baković, M., Vučković, F., Lee, C., Kao, D. H., Wójcik, I., Kliček, F., Polytarchou, C., Roach, B., Louie, T., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.08.034 · Cited by 17 · see citing works
Vedolizumab Does Not Impair Sperm DNA Integrity in Men With Inflammatory Bowel Disease
Grosen, A., Bungum, M., Hvas, C. L., Julsgaard, M., Cordelli, E., & Kelsen, J. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.02.041 · Cited by 16 · see citing works
Introduction to the joint British Society of Gastroenterology (BSG) and Healthcare Infection Society (HIS) faecal microbiota transplant guidelines
Mullish, B. H., Quraishi, M. N., Segal, J. P., Williams, H. R. T., & Goldenberg, S. D. (2018) · Journal of Hospital Infection · doi:10.1016/j.jhin.2018.07.028 · Cited by 12 · see citing works
High prevalence of subclass-specific binding and neutralizing antibodies against Clostridium difficile toxins in adult cystic fibrosis sera: possible mode of immunoprotection against symptomatic C. difficile infection
Monaghan, T. M., Negm, O. H., MacKenzie, B., Hamed, M. R., Shone, C. C., Humphreys, D. P., Acharya, K. R., & Wilcox, M. H. (2017) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s133939 · Cited by 11 · see citing works
Fulminant Clostridium difficile Infection Cured by Fecal Microbiota Transplantation in a Bone Marrow Transplant Recipient With Critical Neutropenia
Krajicek, E. J., Bohm, M., Sagi, S., & Fischer, M. (2019) · ACG Case Reports Journal · doi:10.14309/crj.0000000000000198 · Cited by 9 · see citing works
Effect of sub-MIC of vancomycin and clindamycin alone and in combination with ceftazidime on Clostridium difficile surface layer protein A (slpA) gene expression
Zarandi, E. R., Mansouri, S., Nakhaee, N., Sarafzadeh, F., & Moradi, M. (2017) · Microbial Pathogenesis · doi:10.1016/j.micpath.2017.08.034 · Cited by 7 · see citing works
Is fecal microbiota transplantation a temporary patch for treatment of Clostridium difficile infection or a new frontier of therapeutics?
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Self-citation
Clostridium Difficile Fecal Toxin Level is Associated with Disease Severity and Prognosis
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Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
Cancer and the Microbiome—Influence of the Commensal Microbiota on Cancer, Immune Responses, and Immunotherapy
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A systematic framework for understanding the microbiome in human health and disease: from basic principles to clinical translation
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Health Benefits of Prebiotics, Probiotics, Synbiotics, and Postbiotics
Al-Habsi, N. A., Al‐Khalili, M., Haque, S. A., Elias, M., Olqi, N. A., & Uraimi, T. A. (2024) · Nutrients · doi:10.3390/nu16223955 · Cited by 194 · see citing works
Gut microbiome in modulating immune checkpoint inhibitors
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Antibiotics in Food Chain: The Consequences for Antibiotic Resistance
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Safety and efficacy of fecal microbiota transplantation for treatment of systemic lupus erythematosus: An EXPLORER trial
Huang, C., Yi, P., Zhu, M., Zhou, W., Zhang, B., Yi, X., Long, H., Zhang, G., Wu, H., Tsokos, G. C., et al. (2022) · Journal of Autoimmunity · doi:10.1016/j.jaut.2022.102844 · Cited by 137 · see citing works
Gut microbiome health and dysbiosis: A clinical primer
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Gut microbiome, metabolome, host immunity associated with inflammatory bowel disease and intervention of fecal microbiota transplantation
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Identification of clinical and ecological determinants of strain engraftment after fecal microbiota transplantation using metagenomics
Podlesny, D., Durdevic, M., Paramsothy, S., Kaakoush, N. O., Högenauer, C., Gorkiewicz, G., Walter, J., & Fricke, W. F. (2022) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100711 · Cited by 111 · see citing works
Gut Microbiota Implications for Health and Welfare in Farm Animals: A Review
Chen, S., Luo, S., & Yan, C. (2021) · Animals · doi:10.3390/ani12010093 · Cited by 106 · see citing works
The microbiome in cancer
Lin, A., Xiong, M., Jiang, A., Huang, L., Wong, H. Z. H., Feng, S., Zhang, C., Yu, H., Chen, L., Chi, H., et al. (2025) · iMeta · doi:10.1002/imt2.70070 · Cited by 91 · see citing works
Advances in the integration of metabolomics and metagenomics for human gut microbiome and their clinical applications
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Microbiome-immune interactions in tuberculosis
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Mouse models for bacterial enteropathogen infections: insights into the role of colonization resistance
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Encapsulated Fecal Microbiota Transplantation: Development, Efficacy, and Clinical Application
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Type VI secretion systems of pathogenic and commensal bacteria mediate niche occupancy in the gut
Serapio-Palacios, A., Woodward, S. E., Vogt, S. L., Deng, W., Creus-Cuadros, A., Huus, K. E., Cirstea, M. S., Gerrie, M., Barcik, W., Yu, H., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110731 · Cited by 65 · see citing works
Extracellular Vesicles from Nanomedicine‐Trained Intestinal Microbiota Substitute for Fecal Microbiota Transplant in Treating Ulcerative Colitis
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Fecal Microbiota Transplantation Across the Lifespan: Balancing Efficacy, Safety, and Innovation
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Targeting gut microbiota to alleviate neuroinflammation in Alzheimer’s disease
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Depletion of butyrate-producing microbes of the Firmicutes predicts nonresponse to FMT therapy in patients with recurrent Clostridium difficile infection
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Harness the functions of gut microbiome in tumorigenesis for cancer treatment
Lee, M. (2021) · Cancer Communications · doi:10.1002/cac2.12200 · Cited by 50 · see citing works
Effect of gut flora mediated‐bile acid metabolism on intestinal immune microenvironment
Zhang, Y., Gao, X., Gao, S., Liu, Y., Wang, W., Feng, Y., Pei, L., Sun, Z., Liu, L., & Wang, C. (2023) · Immunology · doi:10.1111/imm.13672 · Cited by 49 · see citing works
Bioengineered Probiotics: Synthetic Biology Can Provide Live Cell Therapeutics for the Treatment of Foodborne Diseases
Cruz, K. C. P., Enekegho, L. O., & Stuart, D. T. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.890479 · Cited by 44 · see citing works
The triple interactions between gut microbiota, mycobiota and host immunity
Yang, J., Yang, H., & Li, Y. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2094888 · Cited by 43 · see citing works
Early gut microbiota intervention in premature infants: Application perspectives
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Probiotics and the Microbiome—How Can We Help Patients Make Sense of Probiotics?
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Domestic Environment and Gut Microbiota: Lessons from Pet Dogs
Hernandez, J. L., Rhimi, S., Kriaa, A., Mariaule, V., Boudaya, H., Drut, A., Jablaoui, A., Mkaouar, H., Saidi, A., Biourge, V. C., et al. (2022) · Microorganisms · doi:10.3390/microorganisms10050949 · Cited by 40 · see citing works
Fecal microbiota transplantation for diseases: Therapeutic potential, methodology, risk management in clinical practice
Qu, Z., Tian, P., Yang, B. K., Zhao, J., Wang, G., & Chen, W. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120719 · Cited by 37 · see citing works
Flavonoid extract of saffron by‐product alleviates hyperuricemia via inhibiting xanthine oxidase and modulating gut microbiota
Chen, N., Wang, R., Li, H., Wang, W., Wang, L., Yin, X., Yao, R., & Yang, B. (2022) · Phytotherapy Research · doi:10.1002/ptr.7579 · Cited by 36 · see citing works
Translational strategies for oral delivery of faecal microbiota transplantation
Kamath, S., Bryant, R. V., Costello, S. P., Day, A. S., Forbes, B., Haifer, C., Hold, G. L., Kelly, C. R., Li, A., Pakuwal, E., et al. (2025) · Gut · doi:10.1136/gutjnl-2025-335077 · Cited by 34 · see citing works
Immune–bacteriophage interactions in inflammatory bowel diseases
Gogokhia, L., & Round, J. L. (2021) · Current Opinion in Virology · doi:10.1016/j.coviro.2021.04.010 · Cited by 34 · see citing works
Prebiotic properties of the polysaccharide from Rosa roxburghii Tratt fruit and its protective effects in high-fat diet-induced intestinal barrier dysfunction: A fecal microbiota transplantation study
Wang, L., Zhang, P., Chen, J., Li, C., Tian, Y., & Xu, F. (2022) · Food Research International · doi:10.1016/j.foodres.2022.112400 · Cited by 33 · see citing works
Faecal (or intestinal) microbiota transplant: a tool for repairing the gut microbiome
Ghani, R., Chrysostomou, D., Roberts, L. A., Pandiaraja, M., Marchesi, J. R., & Mullish, B. H. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2423026 · Cited by 31 · see citing works
Host–Microbiota Interactions in Liver Inflammation and Cancer
Giraud, J., & Saleh, M. (2021) · Cancers · doi:10.3390/cancers13174342 · Cited by 31 · see citing works
Faecal microbiota transplantations and the role of bacteriophages
Liu, Q., Xu, Z., Dai, M. Q., Su, Q., Chan, F. K. L., & Ng, S. C. (2022) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2022.11.012 · Cited by 29 · see citing works
Fecal Microbiota Transplantation Increases Colonic IL-25 and Dampens Tissue Inflammation in Patients with Recurrent Clostridioides difficile
Jan, N., Hays, R. A., Oakland, D. N., Kumar, P., Ramakrishnan, G., Behm, B. W., Petri, W. A., & Marie, C. S. (2021) · mSphere · doi:10.1128/msphere.00669-21 · Cited by 28 · see citing works
The role of short-chain fatty acids in Clostridioides difficile infection: A review
Ouyang, Z.-R., Niu, X.-R., Wang, W., & Zhao, J. (2022) · Anaerobe · doi:10.1016/j.anaerobe.2022.102585 · Cited by 28 · see citing works
Long-Term Safety Following Faecal Microbiota Transplantation as a Treatment for Recurrent Clostridioides difficile Infection Compared with Patients Treated with a Fixed Bacterial Mixture: Results from a Retrospective Cohort Study
Cold, F., Svensson, C. K., Petersen, A. M., Hansen, L. H., & Helms, M. (2022) · Cells · doi:10.3390/cells11030435 · Cited by 27 · see citing works
Pharmacomicrobiomics: Immunosuppressive Drugs and Microbiome Interactions in Transplantation
Mohamed, M. E., Saqr, A., Staley, C. M., Onyeaghala, G. C., Teigen, L. M., Dorr, C. R., Remmel, R. P., Guan, W., Oetting, W. S., Matas, A. J., et al. (2024) · Transplantation · doi:10.1097/tp.0000000000004926 · Cited by 26 · see citing works
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An Update for Pharmacologists on New Treatment Options for Inflammatory Bowel Disease: The Clinicians’ Perspective
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Reply
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Authors: Khoruts, A., Staley, C., & Sadowsky, M. J.
Affiliations: University of Minnesota (US)
Corresponding author: Khoruts, Alexander
ORCID: Khoruts, Alexander
Staley, Christopher
Sadowsky, Michael J.
Venue: Nature Reviews Gastroenterology & Hepatology
Publisher: Springer Science and Business Media LLC
Published: 2020-08-25
Volume: 18
Issue: 1
Pages: 67-80
ISSN: 1759-5045 (ISSN-L)
1759-5053
DOI: 10.1038/s41575-020-0350-4
OpenAlex: W3080453277
Cited by: 155
References: 195
Citations by year: 2026: 19 · 2025: 23 · 2024: 29 · 2023: 22 · 2022: 40 · 2021: 18 · 2020: 4
FWCI: 1.00
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Gastroenterology & Hepatology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: fecal microbiota transplantation, Clostridium difficile infection, recurrent Clostridium difficile infection, pharmacokinetics, pharmacodynamics, microbiota-based therapy
MeSH terms: Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Anti-Bacterial Agents, Clostridium Infections, Feces, Humans, Recurrence, Clostridioides difficile, Treatment Outcome

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Faecal microbiota transplantation for Clostridioides difficile: mechanisms and pharmacology

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