Linking strain engraftment in fecal microbiota transplantation with maintenance of remission in Crohn’s disease
Open accessAbstract
Background & aims Crohn's disease (CD) is a chronic gastrointestinal disease resulting from the dysfunctional interplay between genetic susceptibility, the immune system, and commensal intestinal microbiota. Emerging evidence suggests that treatment by suppression of the immune response and replacement of the microbiota through fecal microbiota transplantation (FMT) is a promising approach for the treatment of CD. Methods We obtained stool metagenomes from CD patients in remission and assessed gut microbiome composition before and after FMT at the species and strain levels. Longitudinal follow-up evaluation allowed us to identify the gain, loss, and strain replacement of specific species and link these events to the maintenance of remission in CD. Results We found that FMT had a significant long-term effect on patient microbial compositions, although this was primarily driven by the engraftment of donor species, which remained at low abundance. Thirty-eight percent of FMT-driven changes were strain replacements, emphasizing the importance of detailed profiling methods, such as metagenomics. Several instances of long-term coexistence between donor and patient strains were also observed. Engraftment of some Actinobacteria, and engraftment or loss of Proteobacteria, were related to better disease outcomes in CD patients who received FMT, and transmission of Bacteroidetes was deleterious. Conclusions Our results suggest clades that may be beneficial to transmit/eliminate through FMT, and provide criteria that may help identify personalized FMT donors to more effectively maintain remission in CD patients. The framework established here creates a foundation for future studies centered around the application of FMT and defined microbial communities as a therapeutic approach for treating CD.
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Following FMT for Crohn disease, engraftment of Haemophilus parainfluenzae and the Enterobacteriaceae member E. coli were associated with disease relapse.
“For example, following FMT for Crohn disease (CD), engraftment of Haemophilus parainfluenzae and the Enterobacteriaceae member E. coli were associated with disease relapse. 85”
From Key determinants of success in fecal microbiota transplantation: From microbiome to clinic (2023) · cites this paper as [85]
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Cites
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
Self-citationphangorn: phylogenetic analysis in R
Schliep, K. P. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq706 · Cited by 3,678 · see citing works
Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases
Lloyd-Price, J., Arze, C., Ananthakrishnan, A. N., Schirmer, M., Avila-Pacheco, J., Poon, T. W., Andrews, E., Ajami, N. J., Bonham, K. S., Brislawn, C. J., et al. (2019) · Nature · doi:10.1038/s41586-019-1237-9 · Cited by 3,143 · see citing works
Self-citationDysfunction of the intestinal microbiome in inflammatory bowel disease and treatment
Morgan, X. C., Tickle, T. L., Sokol, H., Gevers, D., Devaney, K. L., Ward, D. V., Reyes, J. A., Shah, S. A., LeLeiko, N., Snapper, S. B., et al. (2012) · Genome Biology · doi:10.1186/gb-2012-13-9-r79 · Cited by 2,713 · see citing works
Self-citationGenetics and pathogenesis of inflammatory bowel disease
Khor, B., Gardet, A., & Xavier, R. J. (2011) · Nature · doi:10.1038/nature10209 · Cited by 2,630 · see citing works
Self-citationPrecision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile
Buffie, C. G., Bucci, V., Stein, R. R., McKenney, P. T., Ling, L., Gobourne, A., No, D., Liu, H., Kinnebrew, M., Viale, A., et al. (2015) · Nature · doi:10.1038/nature13828 · Cited by 1,872 · see citing works
Metagenomic microbial community profiling using unique clade-specific marker genes
Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O., & Huttenhower, C. (2012) · Nature Methods · doi:10.1038/nmeth.2066 · Cited by 1,776 · see citing works
Species-level functional profiling of metagenomes and metatranscriptomes
Franzosa, E. A., McIver, L. J., Rahnavard, G., Thompson, L. R., Schirmer, M., Weingart, G., Lipson, K. S., Knight, R., Caporaso, J. G., Segata, N., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0176-y · Cited by 1,693 · see citing works
Moayyedi, P., Surette, M. G., Kim, P. T., Libertucci, J., Wolfe, M., Onischi, C., Armstrong, D., Marshall, J. K., Kassam, Z., Reinisch, W., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.04.001 · Cited by 1,499 · see citing works
Paramsothy, S., Kamm, M. A., Kaakoush, N. O., Walsh, A. J., van den Bogaerde, J., Samuel, D., Leong, R. W. L., Connor, S., Ng, W., Paramsothy, R., et al. (2017) · The Lancet · doi:10.1016/s0140-6736(17)30182-4 · Cited by 1,276 · see citing works
Strains, functions and dynamics in the expanded Human Microbiome Project
Lloyd-Price, J., Mahurkar, A., Rahnavard, G., Crabtree, J., Orvis, J., Hall, A. B., Brady, A., Creasy, H. H., McCracken, C., Giglio, M. G., et al. (2017) · Nature · doi:10.1038/nature23889 · Cited by 1,267 · see citing works
Self-citationUnderstanding and Preventing the Global Increase of Inflammatory Bowel Disease
Kaplan, G. G., & Ng, S. C. (2017) · Gastroenterology · doi:10.1053/j.gastro.2016.10.020 · Cited by 1,224 · see citing works
Rossen, N. G., Fuentes, S., van der Spek, M. J., Tijssen, J. G., Hartman, J. H. A., Duflou, A., Löwenberg, M., van den Brink, G. R., Mathus-Vliegen, E. M. H., de Vos, W. M., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.03.045 · Cited by 921 · see citing works
The MetaCyc database of metabolic pathways and enzymes
Caspi, R., Billington, R., Fulcher, C. A., Keseler, I. M., Kothari, A., Krummenacker, M., Latendresse, M., Midford, P. E., Ong, Q., Ong, W. K., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx935 · Cited by 903 · see citing works
Effect of Fecal Microbiota Transplantation on 8-Week Remission in Patients With Ulcerative Colitis
Costello, S. P., Hughes, P. A., Waters, O. R., Bryant, R. V., Vincent, A. D., Blatchford, P. A., Katsikeros, R., Makanyanga, J. C., Campaniello, M. A., Mavrangelos, C., et al. (2019) · JAMA · doi:10.1001/jama.2018.20046 · Cited by 855 · see citing works
Microbial strain-level population structure and genetic diversity from metagenomes
Truong, D. T., Tett, A., Pasolli, E., Huttenhower, C., & Segata, N. (2017) · Genome Research · doi:10.1101/gr.216242.116 · Cited by 839 · see citing works
A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients
Hall, A. B., Yassour, M., Sauk, J., Garner, A., Jiang, X., Arthur, T., Lagoudas, G. K., Vatanen, T., Fornelos, N., Wilson, R., et al. (2017) · Genome Medicine · doi:10.1186/s13073-017-0490-5 · Cited by 777 · see citing works
Self-citationCancers Complicating Inflammatory Bowel Disease
Beaugerie, L., & Itzkowitz, S. H. (2015) · New England Journal of Medicine · doi:10.1056/nejmra1403718 · Cited by 681 · see citing works
Self-citationKirchgesner, J., Lemaître, M., Carrat, F., Zureik, M., Carbonnel, F., & Dray‐Spira, R. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.04.012 · Cited by 610 · see citing works
Maldonado-Gómez, M. X., Martínez, I., Bottacini, F., O’Callaghan, A., Ventura, M., van Sinderen, D., Hillmann, B., Vangay, P., Knights, D., Hutkins, R. W., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.09.001 · Cited by 517 · see citing works
Ananthakrishnan, A. N., Luo, C., Yajnik, V., Khalili, H., Garber, J. J., Stevens, B. W., Cleland, T., & Xavier, R. J. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.04.010 · Cited by 451 · see citing works
Self-citationParamsothy, S., Paramsothy, R., Rubin, D. T., Kamm, M. A., Kaakoush, N. O., Mitchell, H. M., & Castaño-Rodríguez, N. (2017) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjx063 · Cited by 436 · see citing works
The Super-Donor Phenomenon in Fecal Microbiota Transplantation
Wilson, B. C., Vatanen, T., Cutfield, W. S., & O'Sullivan, J. M. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00002 · Cited by 420 · see citing works
Self-citationRole of the Gut Microbiome in Uremia: A Potential Therapeutic Target
Ramezani, A., Massy, Z. A., Meijers, B., Evenepoel, P., Vanholder, R., & Raj, D. S. (2016) · American Journal of Kidney Diseases · doi:10.1053/j.ajkd.2015.09.027 · Cited by 394 · see citing works
Saint-Antoine IBD Network, Sokol, H., Landman, C., Seksik, P., Berard, L., Montil, M., Nion-Larmurier, I., Bourrier, A., Le Gall, G., Lalande, V., et al. (2020) · Microbiome · doi:10.1186/s40168-020-0792-5 · Cited by 378 · see citing works
Self-citationAn exclusive metabolic niche enables strain engraftment in the gut microbiota
Shepherd, E. S., DeLoache, W. C., Pruss, K. M., Whitaker, W. R., & Sonnenburg, J. L. (2018) · Nature · doi:10.1038/s41586-018-0092-4 · Cited by 367 · see citing works
Plichta, D. R., Graham, D. B., Subramanian, S., & Xavier, R. J. (2019) · Cell · doi:10.1016/j.cell.2019.07.045 · Cited by 313 · see citing works
Self-citationMicrobiota-derived lantibiotic restores resistance against vancomycin-resistant Enterococcus
Kim, S. G., Becattini, S., Moody, T. U., Shliaha, P. V., Littmann, E. R., Seok, R., Gjonbalaj, M., Eaton, V. P., Fontana, E., Amoretti, L. A., et al. (2019) · Nature · doi:10.1038/s41586-019-1501-z · Cited by 280 · see citing works
Host-microbial Cross-talk in Inflammatory Bowel Disease
Nagao‐Kitamoto, H., & Kamada, N. (2017) · Immune Network · doi:10.4110/in.2017.17.1.1 · Cited by 179 · see citing works
Fischer, M., Kao, D. H., Kelly, C. R., Kuchipudi, A., Jafri, S., Blumenkehl, M., Rex, D. K., Mellow, M., Kaur, N. J., Sokol, H., et al. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000908 · Cited by 178 · see citing works
Self-citationKhanna, S., Vázquez‐Baeza, Y., González, A., Weiss, S. J., Schmidt, B. A., Pedrogo, D. A. M., Rainey, J. F., Kammer, P. P., Nelson, H., Sadowsky, M. J., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0269-3 · Cited by 163 · see citing works
Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns
Pamer, E. G. (2014) · Mucosal Immunology · doi:10.1038/mi.2013.117 · Cited by 109 · see citing works
The Gut Microbiota in Inflammatory Bowel Disease
Macfarlane, G. T., Blackett, K. L., Nakayama, T., Steed, H., & Macfarlane, S. (2009) · Current Pharmaceutical Design · doi:10.2174/138161209788168146 · Cited by 108 · see citing works
Orthogonal Dietary Niche Enables Reversible Engraftment of a Gut Bacterial Commensal
Kearney, S. M., Gibbons, S. M., Erdman, S. E., & Alm, E. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.032 · Cited by 93 · see citing works
Staley, C. M., Kaiser, T., Vaughn, B. P., Graiziger, C. T., Hamilton, M. J., Kabage, A. J., Khoruts, A., & Sadowsky, M. J. (2019) · mBio · doi:10.1128/mbio.01586-19 · Cited by 84 · see citing works
Hirten, R. P., Grinspan, A. M., Fu, S., Luo, Y., Suárez‐Fariñas, M., Rowland, J., Contijoch, E. J., Mogno, I., Yang, N., Luong, T., et al. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy398 · Cited by 56 · see citing works
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Ianiro, G., Punčochář, M., Karcher, N., Porcari, S., Armanini, F., Asnicar, F., Beghini, F., Blanco-Míguez, A., Cumbo, F., Manghi, P., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01964-3 · Cited by 366 · see citing works
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
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- Authors
- Kong, L., Lloyd-Price, J., Vatanen, T., Seksik, P., Beaugerie, L., Simon, T., Vlamakis, H., Sokol, H., & Xavier, R. J.
- Affiliations
- Broad Institute (US)
- Inserm (FR)
- Assistance Publique – Hôpitaux de Paris (FR)
- Corresponding author
- Sokol, Harry
- Xavier, Ramnik J.
- ORCID
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2020-12
- Volume
- 159
- Issue
- 6
- Pages
- 2193-2202.e5
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC7725862
- OpenAlex
- W3081352202
- Cited by
- 69
- References
- 36
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 11 · 2023: 13 · 2022: 17 · 2021: 12
- FWCI
- 3.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Gastroenterology (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, cc-by-nc)
- ResearchSpace (University of Auckland) (submittedVersion)
- Funders
- AbbVie
- Assistance publique-Hôpitaux de Paris (CRC16)
- Meso Scale Diagnostics
- Takeda Pharmaceutical Company
- Janssen Pharmaceuticals
- Ferring Pharmaceuticals
- Astellas Pharma US
- Horizon 2020 (ERC-2016-StG-71577)
- National Institutes of Health (AT009708)
- European Research Council
- Abbott Laboratories
- Fondation de France
- Amgen
- Ministère de la Santé
- Pfizer
- Horizon 2020 Framework Programme
- Crohn's and Colitis Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
- Keywords
- fecal microbiota transplantation, Crohn's disease, remission maintenance, gut microbiota, strain replacement, actinobacteria, Proteobacteria, Bacteroidetes, stool metagenomics
- MeSH terms
- Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Adult, Crohn Disease, Feces, Female, Haplotypes, Humans, Male, Middle Aged, Phylogeny, Remission Induction, Treatment Outcome, Young Adult, Metagenomics, Molecular Typing, Datasets as Topic
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