The super-donor phenomenon in fecal microbiota transplantation

Frontiers in Cellular and Infection Microbiology

Volumn 9, Issue JAN, 2019, Pages

  Wilson, Brooke C ^a   Vatanen, Tommi ^a,b   Cutfield, Wayne S ^a   O'Sullivan, Justin M ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

Clostridium difficile infection (CDI); Fecal microbiota transplantation (FMT); Inflammatory bowel disease (IBD); Microbial dysbiosis; Super donor

Indexed keywords

LACTULOSE; RIFAXIMIN;

CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; CONSTIPATION; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL DISEASE; HEPATIC ENCEPHALOPATHY; HUMAN; IMMUNE RESPONSE; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIAL INTERACTION; MICROBIOLOGICAL PARAMETERS; PEPTOCLOSTRIDIUM DIFFICILE; REVIEW; SUPER DONOR PHENOMENON; CLOSTRIDIUM INFECTION; DONOR; MICROFLORA; PROCEDURES;

CLOSTRIDIUM INFECTIONS; FECAL MICROBIOTA TRANSPLANTATION; GASTROINTESTINAL MICROBIOME; HUMANS; MICROBIOTA; TISSUE DONORS;

EID: 85061053895     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2019.00002     Document Type: Review

References (130)

1. Aroniadis, O. C., Brandt, L. J., Oneto, C., Feuerstadt, P., Sherman, A., Wolkoff, A. W., et al. (2018). 742 - A double-blind, randomized, placebo-controlled trial of fecal microbiota transplantation capsules (FMTC) for the treatment of diarrhea-predominant irritable bowel syndrome (IBS-D). Gastroenterology 154, S-154-S-155. doi: 10.1016/S0016-5085(18)30932-6
2. Arrieta, M. C., Stiemsma, L. T., Dimitriu, P. A., Thorson, L., Russell, S., Yurist-Doutsch, S., et al. (2015). Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci. Transl. Med. 7:307ra152. doi: 10.1126/scitranslmed.aab2271
3. Bäckhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., et al. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci.U.S.A. 101, 15718-15723. doi: 10.1073/pnas.0407076101
4. Bajaj, J. S., Kassam, Z., Fagan, A., Gavis, E. A., Liu, E., Cox, I. J., et al. (2017). Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology 66, 1727-1738. doi: 10.1002/hep.29306
5. Balish, E., and Warner, T. (2002). Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am. J. Pathol. 160, 2253-2257. doi: 10.1016/S0002-9440(10)61172-8
6. Baumgart, M., Dogan, B., Rishniw, M., Weitzman, G., Bosworth, B., Yantiss, R., et al. (2007). Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 1, 403-418. doi: 10.1038/ismej.2007.52
7. Belkaid, Y., and Hand, T. W. (2014). Role of the microbiota in immunity and inflammation. Cell 157, 121-141. doi: 10.1016/j.cell.2014.03.011
8. Bennet, J. D., and Brinkman, M. (1989). Treatment of 'ulcerative colitis by implantation of normal colonic flora. Lancet 1:164. doi: 10.1016/S0140-6736(89)91183-5
9. Berer, K., Mues, M., Koutrolos, M., Rasbi, Z. A., Boziki, M., Johner, C., et al. (2011). Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479, 538-541. doi: 10.1038/nature10554
10. Borriello, S. P. (1990). The influence of the normal flora on Clostridium difficile colonisation of the gut. Ann. Med. 22, 61-67. doi: 10.3109/07853899009147244
11. Broecker, F., Klumpp, J., Schuppler, M., Russo, G., Biedermann, L., Hombach, M., et al. (2016). Long-term changes of bacterial and viral compositions in the intestine of a recovered Clostridium difficile patient after fecal microbiota transplantation. Cold Spring Harb. Mol. Case Stud. 2:a000448. doi: 10.1101/mcs.a000448
12. Bunyavanich, S., Shen, N., Grishin, A., Wood, R., Burks, W., Dawson, P., et al. (2016). Early-life gut microbiome composition and milk allergy resolution. J. Allergy Clin. Immunol. 138, 1122-1130. doi: 10.1016/j.jaci.2016.03.041
13. Cammarota, G., Ianiro, G., Tilg, H., Rajilić-Stojanović, M., Kump, P., Satokari, R., et al. (2017). European consensus conference on faecal microbiota transplantation in clinical practice. Gut 66, 569-580. doi: 10.1136/gutjnl-2016-313017
14. Cammarota, G., Masucci, L., Ianiro, G., Bibbò, S., Dinoi, G., Costamagna, G., et al. (2015). Randomised clinical trial: faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection. Aliment. Pharmacol. Ther. 41, 835-843. doi: 10.1111/apt.13144
15. Chen, Y., Yang, F., Lu, H., Wang, B., Chen, Y., Lei, D., et al. (2011). Characterization of fecal microbial communities in patients with liver cirrhosis. Hepatology 54, 562-572. doi: 10.1002/hep.24423
16. Conceição-Neto, N., Deboutte, W., Dierckx, T., Machiels, K., Wang, J., Yinda, K. C., et al. (2018). Low eukaryotic viral richness is associated with faecal microbiota transplantation success in patients with UC. Gut 67, 1558-1559. doi: 10.1136/gutjnl-2017-315281
17. Costello, S. P., Soo, W., Bryant, R. V., Jairath, V., Hart, A. L., and Andrews, J. M. (2017). Systematic review with meta-analysis: faecal microbiota transplantation for the induction of remission for active ulcerative colitis. Aliment. Pharmacol. Ther. 46, 213-224. doi: 10.1111/apt.14173
18. Cui, B., Feng, Q., Wang, H., Wang, M., Peng, Z., Li, P., et al. (2015). Fecal microbiota transplantation through mid-gut for refractory Crohn's disease: safety, feasibility, and efficacy trial results. J. Gastroenterol. Hepatol. 30, 51-58. doi: 10.1111/jgh.12727
19. Cui, L., Zhao, T., Hu, H., Zhang, W., and Hua, X. (2017). Association study of gut flora in coronary heart disease through high-throughput sequencing. Biomed. Res. Int. 2017:3796359. doi: 10.1155/2017/3796359
20. Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A. L., Barnich, N., et al. (2004). High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127, 412-421. doi: 10.1053/j.gastro.2004.04.061
21. David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., et al. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563. doi: 10.1038/nature12820
22. de Groot, P. F., Frissen, M. N., de Clercq, N. C., and Nieuwdorp, M. (2017). Fecal microbiota transplantation in metabolic syndrome: history, present and future. Gut Microbes 8, 253-267. doi: 10.1080/19490976.2017.1293224
23. de Lange, K. M., Moutsianas, L., Lee, J. C., Lamb, C. A., Luo, Y., Kennedy, N. A., et al. (2017). Genome-wide association study implicates immune activation of multiple integrin genes in inflammatory bowel disease. Nat. Genet. 49, 256-261. doi: 10.1038/ng.3760
24. DeFilipp, Z., Peled, J. U., Li, S., Mahabamunuge, J., Dagher, Z., Slingerland, A. E., et al. (2018). Third-party fecal microbiota transplantation following allo-HCT reconstitutes microbiome diversity. Blood Adv. 2, 745-753. doi: 10.1182/bloodadvances.2018017731
25. Ding, C., Fan, W., Gu, L., Tian, H., Ge, X., Gong, J., et al. (2018). Outcomes and prognostic factors of fecal microbiota transplantation in patients with slow transit constipation: results from a prospective study with long-term follow-up. Gastroenterol. Rep. 6, 101-107. doi: 10.1093/gastro/gox036
26. Duvallet, C., Gibbons, S. M., Gurry, T., Irizarry, R. A., and Alm, E. J. (2017). Meta-analysis of gut microbiome studies identifies disease-specific and shared responses. Nat. Commun. 8:1784. doi: 10.1038/s41467-017-01973-8
27. Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., et al. (2005). Diversity of the human intestinal microbial flora. Science 308, 1635-1638. doi: 10.1126/science.1110591
28. Eiseman, B., Silen, W., Bascom, G. S., and Kauvar, A. J. (1958). Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44, 854-859.
29. Emanuelsson, F., Claesson, B. E., Ljungström, L., Tvede, M., and Ung, K. A. (2014). Faecal microbiota transplantation and bacteriotherapy for recurrent Clostridium difficile infection: a retrospective evaluation of 31 patients. Scand. J. Infect. Dis. 46, 89-97. doi: 10.3109/00365548.2013.858181
30. Fekety, R., McFarland, L. V., Surawicz, C. M., Greenberg, R. N., Elmer, G. W., and Mulligan, M. E. (1997). Recurrent Clostridium difficile diarrhea: characteristics of and risk factors for patients enrolled in a prospective, randomized, double-blinded trial. Clin. Infect. Dis. 24, 324-333. doi: 10.1093/clinids/24.3.324
31. Frank, D. N., St. Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., and Pace, N. R. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci.U.S.A. 104, 13780-13785. doi: 10.1073/pnas.0706625104
32. Fuentes, S., Rossen, N. G., van der Spek, M. J., Hartman, J. H., Huuskonen, L., Korpela, K., et al. (2017). Microbial shifts and signatures of long-term remission in ulcerative colitis after faecal microbiota transplantation. ISME J. 11, 1877-1889. doi: 10.1038/ismej.2017.44
33. Fujimoto, T., Imaeda, H., Takahashi, K., Kasumi, E., Bamba, S., Fujiyama, Y., et al. (2013). Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn's disease. J. Gastroenterol. Hepatol. 28, 613-619. doi: 10.1111/jgh.12073
34. Gajendran, M., Loganathan, P., Catinella, A. P., and Hashash, J. G. (2018). A comprehensive review and update on Crohn's disease. Dis. Mon. 64, 20-57. doi: 10.1016/j.disamonth.2017.07.001
35. Gevers, D., Kugathasan, S., Denson, L. A., Vázquez-Baeza, Y., Van Treuren, W., Ren, B., et al. (2014). The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15, 382-392. doi: 10.1016/j.chom.2014.02.005
36. Goodrich, J. K., Davenport, E. R., Beaumont, M., Jackson, M. A., Knight, R., Ober, C., et al. (2016). Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731-743. doi: 10.1016/j.chom.2016.04.017
37. Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., et al. (2014). Human genetics shape the gut microbiome. Cell 159, 789-799. doi: 10.1016/j.cell.2014.09.053
38. Goyal, A., Yeh, A., Bush, B. R., Firek, B. A., Siebold, L. M., Rogers, M. B., et al. (2018). Safety, clinical response, and microbiome findings following fecal microbiota transplant in children with inflammatory bowel disease. Inflamm. Bowel Dis. 24, 410-421. doi: 10.1093/ibd/izx035
39. Halkjær, S. I., Christensen, A. H., Lo, B. Z. S., Browne, P. D., Günther, S., Hansen, L. H., et al. (2018). Faecal microbiota transplantation alters gut microbiota in patients with irritable bowel syndrome: results from a randomised, double-blind placebo-controlled study. Gut 67, 2107-2115. doi: 10.1136/gutjnl-2018-316434
40. Hall, A. B., Tolonen, A. C., and Xavier, R. J. (2017). Human genetic variation and the gut microbiome in disease. Nat. Rev. Genet. 18, 690-699. doi: 10.1038/nrg.2017.63
41. He, Z., Cui, B. T., Zhang, T., Li, P., Long, C. Y., Ji, G. Z., et al. (2017a). Fecal microbiota transplantation cured epilepsy in a case with Crohn's disease: the first report. World J. Gastroenterol. 23, 3565-3568. doi: 10.3748/wjg.v23.i19.3565
42. He, Z., Li, P., Zhu, J., Cui, B., Xu, L., Xiang, J., et al. (2017b). Multiple fresh fecal microbiota transplants induces and maintains clinical remission in Crohn's disease complicated with inflammatory mass. Sci Rep. 7:4753. doi: 10.1038/s41598-017-04984-z
43. Holvoet, T., Joossens, M., Boelens, J., Christiaens, E., Heyerick, L., Verhasselt, B., et al. (2018). 617 - fecal microbiota transplantation in irritable bowel syndrome with predominant abdominal bloating: results from a double blind, placebo-controlled clinical trial. Gastroenterology 154:S-130. doi: 10.1016/S0016-5085(18)30860-6
44. Holvoet, T., Joossens, M., Wang, J., Boelens, J., Verhasselt, B., Laukens, D., et al. (2017). Assessment of faecal microbial transfer in irritable bowel syndrome with severe bloating. Gut 66, 980-982. doi: 10.1136/gutjnl-2016-312513
45. Human Microbiome Project Consortium. (2012). Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214. doi: 10.1038/nature11234
46. Ishikawa, D., Sasaki, T., Osada, T., Kuwahara-Arai, K., Haga, K., Shibuya, T., et al. (2017). Changes in intestinal microbiota following combination therapy with fecal microbial transplantation and antibiotics for Ulcerative Colitis. Inflamm. Bowel Dis. 23, 116-125. doi: 10.1097/MIB.0000000000000975
47. Jie, Z., Xia, H., Zhong, S. L., Feng, Q., Li, S., Liang, S., et al. (2017). The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun. 8:845. doi: 10.1038/s41467-017-00900-1
48. Johnsen, P. H., Hilpüsch, F., Cavanagh, J. P., Leikanger, I. S., Kolstad, C., Valle, P. C., et al. (2018). Faecal microbiota transplantation versus placebo for moderate-to-severe irritable bowel syndrome: a double-blind, randomised, placebo-controlled, parallel-group, single-centre trial. Lancet Gastroenterol. Hepatol. 3, 17-24. doi: 10.1016/S2468-1253(17)30338-2
49. Kakihana, K., Fujioka, Y., Suda, W., Najima, Y., Kuwata, G., Sasajima, S., et al. (2016). Fecal microbiota transplantation for patients with steroid-resistant acute graft-versus-host disease of the gut. Blood 128, 2083-2088. doi: 10.1182/blood-2016-05-717652
50. Kang, D. W., Adams, J. B., Gregory, A. C., Borody, T., Chittick, L., Fasano, A., et al. (2017). Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5:10. doi: 10.1186/s40168-016-0225-7
51. Kao, D., Roach, B., Park, H., Hotte, N., Madsen, K., Bain, V., et al. (2016). Fecal microbiota transplantation in the management of hepatic encephalopathy. Hepatology 63, 339-340. doi: 10.1002/hep.28121
52. Kao, D., Roach, B., Silva, M., Beck, P., Rioux, K., Kaplan, G. G., et al. (2017). Effect of oral capsule- vs colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection. JAMA 318:1985. doi: 10.1001/jama.2017.17077
53. Kassam, Z., Lee, C. H., Yuan, Y., and Hunt, R. H. (2013). Fecal Microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am. J. Gastroenterol. 108, 500-508. doi: 10.1038/ajg.2013.59
54. Kazerouni, A., and Wein, L. M. (2017). Exploring the efficacy of pooled stools in fecal microbiota transplantation for microbiota-associated chronic diseases. PLoS ONE 12:e0163956. doi: 10.1371/journal.pone.0163956
55. Kellingray, L., Gall, G. L., Defernez, M., Beales, I. L. P., Franslem-Elumogo, N., and Narbad, A. (2018). Microbial taxonomic and metabolic alterations during faecal microbiota transplantation to treat Clostridium difficile infection. J. Infect. 77, 107-118. doi: 10.1016/j.jinf.2018.04.012
56. Kelly, C. R., Kahn, S., Kashyap, P., Laine, L., Rubin, D., Atreja, A., et al. (2015). Update on fecal microbiota transplantation: indications, methodologies, mechanisms, and outlook. Gastroenterology 149, 223-237. doi: 10.1053/j.gastro.2015.05.008
57. Kelly, C. R., Khoruts, A., Staley, C., Sadowsky, M. J., Abd, M., Alani, M., et al. (2016). Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection. Ann. Intern. Med. 165, 609-616. doi: 10.7326/M16-0271
58. Khanna, S. (2018). Microbiota replacement therapies: innovation in gastrointestinal care. Clin. Pharmacol. Ther. 103, 102-111. doi: 10.1002/cpt.923
59. Khanna, S., Vazquez-Baeza, Y., González, A., Weiss, S., Schmidt, B., Muñiz-Pedrogo, D. A., et al. (2017). Changes in microbial ecology after fecal microbiota transplantation for recurrent C. difficile infection affected by underlying inflammatory bowel disease. Microbiome 5:55. doi: 10.1186/s40168-017-0269-3
60. Koh, A., De Vadder, F., Kovatcheva-Datchary, P., and Bäckhed, F. (2016). From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165, 1332-1345. doi: 10.1016/j.cell.2016.05.041
61. Kootte, R. S., Levin, E., Salojärvi, J., Smits, L. P., Hartstra, A. V., Udayappan, S. D., et al. (2017). Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. 26, 611-619.e6. doi: 10.1016/j.cmet.2017.09.008
62. Kriss, M., Hazleton, K. Z., Nusbacher, N. M., Martin, C. G., and Lozupone, C. A. (2018). Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Curr. Opin. Microbiol. 44, 34-40. doi: 10.1016/j.mib.2018.07.003
63. Kumar, R., Yi, N., Zhi, D., Eipers, P., Goldsmith, K. T., Dixon, P., et al. (2017). Identification of donor microbe species that colonize and persist long term in the recipient after fecal transplant for recurrent Clostridium difficile. npj Biofilms Microb. 3:12. doi: 10.1038/s41522-017-0020-7
64. Kump, P., Wurm, P., Gröchenig, H. P., Wenzl, H., Petritsch, W., Halwachs, B., et al. (2018). The taxonomic composition of the donor intestinal microbiota is a major factor influencing the efficacy of faecal microbiota transplantation in therapy refractory ulcerative colitis. Aliment. Pharmacol. Ther. 47, 67-77. doi: 10.1111/apt.14387
65. Lee, C. H., Belanger, J. E., Kassam, Z., Smieja, M., Higgins, D., Broukhanski, G., et al. (2014). The outcome and long-term follow-up of 94 patients with recurrent and refractory Clostridium difficile infection using single to multiple fecal microbiota transplantation via retention enema. Eur. J. Clin. Microbiol. Infect. Dis. 33, 1425-1428. doi: 10.1007/s10096-014-2088-9
66. Lee, C. H., Steiner, T., Petrof, E. O., Smieja, M., Roscoe, D., Nematallah, A., et al. (2016). Frozen vs fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection. JAMA 315, 142-149. doi: 10.1001/jama.2015.18098
67. Leffler, D. A., and Lamont, J. T. (2015). Clostridium difficile infection. N Engl J Med. 372, 1539-1548. doi: 10.1056/NEJMra1403772
68. Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., et al. (2008). Evolution of mammals and their gut microbes. Science 320, 1647-1651. doi: 10.1126/science.1155725
69. Li, S. S., Zhu, A., Benes, V., Costea, P. I., Hercog, R., Hildebrand, F., et al. (2016). Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science 352, 586-589. doi: 10.1126/science.aad8852
70. Liu, H. N., Wu, H., Chen, Y. Z., Chen, Y. J., Shen, X. Z., and Liu, T. T. (2017). Altered molecular signature of intestinal microbiota in irritable bowel syndrome patients compared with healthy controls: a systematic review and meta-analysis. Dig. Liver Dis. 49, 331-337. doi: 10.1016/j.dld.2017.01.142
71. Liu, S. X., Li, Y. H., Dai, W. K., Li, X. S., Qiu, C. Z., Ruan, M. L., et al. (2017). Fecal microbiota transplantation induces remission of infantile allergic colitis through gut microbiota re-establishment. World J. Gastroenterol. 23, 8570-8581. doi: 10.3748/wjg.v23.i48.8570
72. Lloyd-Price, J., Abu-Ali, G., and Huttenhower, C. (2016). The healthy human microbiome. Genome Med. 8:51. doi: 10.1186/s13073-016-0307-y
73. Lopez-Siles, M., Martinez-Medina, M., Abellà, C., Busquets, D., Sabat-Mir, M., Duncan, S. H., et al. (2015). Mucosa-associated Faecalibacterium prausnitzii phylotype richness is reduced in patients with inflammatory bowel disease. Appl. Environ. Microbiol. 81, 7582-7592. doi: 10.1128/AEM.02006-15
74. Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., et al. (2014). A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63, 1275-1283. doi: 10.1136/gutjnl-2013-304833
75. Makkawi, S., Camara-Lemarroy, C., and Metz, L. (2018). Fecal microbiota transplantation associated with 10 years of stability in a patient with SPMS. Neurol. Neuroimmunol. Neuroinflamm. 5:e459. doi: 10.1212/NXI.0000000000000459
76. Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., et al. (2006). Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55, 205-211. doi: 10.1136/gut.2005.073817
77. Martin, H. M., Campbell, B. J., Hart, C. A., Mpofu, C., Nayar, M., Singh, R., et al. (2004). Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 127, 80-93. doi: 10.1053/j.gastro.2004.03.054
78. Mattila, E., Uusitalo-Seppälä, R., Wuorela, M., Lehtola, L., Nurmi, H., Ristikankare, M., et al. (2012). Fecal transplantation, through colonoscopy, is effective therapy for recurrent Clostridium difficile infection. Gastroenterology 142, 490-496. doi: 10.1053/j.gastro.2011.11.037
79. Mizuno, S., Masaoka, T., Naganuma, M., Kishimoto, T., Kitazawa, M., Kurokawa, S., et al. (2017). Bifidobacterium-rich fecal donor may be a positive predictor for successful fecal microbiota transplantation in patients with irritable bowel syndrome. Digestion 96, 29-38. doi: 10.1159/000471919
80. Moayyedi, P., Surette, M. G., Kim, P. T., Libertucci, J., Wolfe, M., Onischi, C., et al. (2015). Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149, 102-109.e6. doi: 10.1053/j.gastro.2015.04.001
81. Moss, E. L., Falconer, S. B., Tkachenko, E., Wang, M., Systrom, H., Mahabamunuge, J., et al. (2017). Long-term taxonomic and functional divergence from donor bacterial strains following fecal microbiota transplantation in immunocompromised patients. PLoS ONE 12:e0182585. doi: 10.1371/journal.pone.0182585
82. Ni, J., Wu, G. D., Albenberg, L., and Tomov, V. T. (2017). Gut microbiota and IBD: causation or correlation? Nat. Rev. Gastroenterol. Hepatol. 14, 573-584. doi: 10.1038/nrgastro.2017.88
83. Nishida, A., Imaeda, H., Ohno, M., Inatomi, O., Bamba, S., Sugimoto, M., et al. (2017). Efficacy and safety of single fecal microbiota transplantation for Japanese patients with mild to moderately active ulcerative colitis. J. Gastroenterol. 52, 476-482. doi: 10.1007/s00535-016-1271-4
84. Nishino, K., Nishida, A., Inoue, R., Kawada, Y., Ohno, M., Sakai, S., et al. (2018). Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J. Gastroenterol. 53, 95-106. doi: 10.1007/s00535-017-1384-4
85. Odamaki, T., Kato, K., Sugahara, H., Hashikura, N., Takahashi, S., Xiao, J. Z., et al. (2016). Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 16:90. doi: 10.1186/s12866-016-0708-5
86. Osman, M., Stoltzner, Z., O'Brien, K., Ling, K., Koelsch, E., Dubois, N., et al. (2016). Donor efficacy in fecal microbiota transplantation for recurrent clostridium difficile: evidence from a 1,999-patient cohort. Open Forum Infect. Dis. 3, 841. doi: 10.1093/ofid/ofw194.48
87. Ott, S. J., Waetzig, G. H., Rehman, A., Moltzau-Anderson, J., Bharti, R., Grasis, J. A., et al. (2017). Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology 152, 799-811.e7. doi: 10.1053/j.gastro.2016.11.010
88. Paramsothy, S., Kamm, M. A., Kaakoush, N. O., Walsh, A. J., van den Bogaerde, J., Samuel, D., et al. (2017a). Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet 389, 1218-1228. doi: 10.1016/S0140-6736(17)30182-4
89. Paramsothy, S., Paramsothy, R., Rubin, D. T., Kamm, M. A., Kaakoush, N. O., Mitchell, H. M., et al. (2017b). Faecal microbiota transplantation for inflammatory bowel disease: a systematic review and meta-analysis. J. Crohn's Colitis 11, 1180-1199. doi: 10.1093/ecco-jcc/jjx063
90. Penders, J., Thijs, C., van den Brandt, P. A., Kummeling, I., Snijders, B., Stelma, F., et al. (2007). Gut microbiota composition and development of atopic manifestations in infancy: the KOALA birth Cohort study. Gut 56, 661-667. doi: 10.1136/gut.2006.100164
91. Perez-Muñoz, M. E., Arrieta, M.-C., Ramer-Tait, A. E., and Walter, J. (2017). A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome 5:48. doi: 10.1186/s40168-017-0268-4
92. Petersen, C., and Round, J. L. (2014). Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 16, 1024-1033. doi: 10.1111/cmi.12308
93. Petrof, E. O., Gloor, G. B., Vanner, S. J., Weese, S. J., Carter, D., Daigneault, M. C., et al. (2013). Stool substitute transplant therapy for the eradication of Clostridium difficile infection: 'RePOOPulating' the gut. Microbiome 1:3. doi: 10.1186/2049-2618-1-3
94. Philips, C. A., Pande, A., Shasthry, S. M., Jamwal, K. D., Khillan, V., Chandel, S. S., et al. (2017). Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin. Gastroenterol. Hepatol. 15, 600-602. doi: 10.1016/j.cgh.2016.10.029
95. Pinn, D. M., Aroniadis, O. C., and Brandt, L. J. (2014). Is fecal microbiota transplantation the answer for irritable bowel syndrome? A single-center experience. Am. J. Gastroenterol. 109, 1831-1832. doi: 10.1038/ajg.2014.295
96. Ponce-Alonso, M., Garcia-Fernandez, S., Aguilera, L., Rodriguez de santiago, E., Foruny, J. R., Roy, G., et al. (2017). P782 A new compatibility test for donor selection for faecal microbiota transplantation in ulcerative colitis. J Crohn's Colitis 11, S480-S481. doi: 10.1093/ecco-jcc/jjx002.903
97. Quraishi, M. N., Widlak, M., Bhala, N., Moore, D., Price, M., Sharma, N., et al. (2017). Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment. Pharmacol. Ther. 46, 479-493. doi: 10.1111/apt.14201
98. Ren, Y. D., Ye, Z. S., Yang, L. Z., Jin, L. X., Wei, W. J., Deng, Y. Y., et al. (2017). Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology 65, 1765-1768. doi: 10.1002/hep.29008
99. Ridaura, V. K., Faith, J. J., Rey, F. E., Cheng, J., Duncan, A. E., Kau, A. L., et al. (2013). Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214. doi: 10.1126/science.1241214
100. Rossen, N. G., Fuentes, S., van der Spek, M. J., Tijssen, J. G., Hartman, J. H., Duflou, A., et al. (2015). Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 149, 110-118.e4. doi: 10.1053/j.gastro.2015.03.045
101. Schaubeck, M., Clavel, T., Calasan, J., Lagkouvardos, I., Haange, S. B., Jehmlich, N., et al. (2016). Dysbiotic gut microbiota causes transmissible Crohn's disease-like ileitis independent of failure in antimicrobial defence. Gut 65, 225-237. doi: 10.1136/gutjnl-2015-309333
102. Schwiertz, A., Taras, D., Schäfer, K., Beijer, S., Bos, N. A., Donus, C., et al. (2010). Microbiota and SCFA in lean and overweight healthy subjects. Obesity 18, 190-195. doi: 10.1038/oby.2009.167
103. Sellon, R. K., Tonkonogy, S., Schultz, M., Dieleman, L. A., Grenther, W., Balish, E., et al. (1998). Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66, 5224-5231.
104. Shankar, V., Hamilton, M. J., Khoruts, A., Kilburn, A., Unno, T., Paliy, O., et al. (2014). Species and genus level resolution analysis of gut microbiota in Clostridium difficile patients following fecal microbiota transplantation. Microbiome 2:13. doi: 10.1186/2049-2618-2-13
105. Singh, R. K., Chang, H. W., Yan, D., Lee, K. M., Ucmak, D., Wong, K., et al. (2017). Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 15:73. doi: 10.1186/s12967-017-1175-y
106. Smillie, C. S., Sauk, J., Gevers, D., Friedman, J., Sung, J., Youngster, I., et al. (2018). Strain tracking reveals the determinants of bacterial engraftment in the human gut following fecal microbiota transplantation. Cell Host Microbe. 23, 229-240.e5. doi: 10.1016/j.chom.2018.01.003
107. Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J. J., et al. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U S A. 105, 16731-16736. doi: 10.1073/pnas.0804812105
108. Song, Y., Garg, S., Girotra, M., Maddox, C., von Rosenvinge, E. C., Dutta, A., et al. (2013). Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent Clostridium difficile infection. PLoS ONE. 8:e81330. doi: 10.1371/journal.pone.0081330
109. Spindelboeck, W., Schulz, E., Uhl, B., Kashofer, K., Aigelsreiter, A., Zinke-Cerwenka, W., et al. (2017). Repeated fecal microbiota transplantations attenuate diarrhea and lead to sustained changes in the fecal microbiota in acute, refractory gastrointestinal graft-versus-host-disease. Haematologica 102, e210-e213. doi: 10.3324/haematol.2016.154351
110. Staley, C., Kelly, C. R., Brandt, L. J., Khoruts, A., and Sadowsky, M. J. (2016). Complete microbiota engraftment is not essential for recovery from recurrent Clostridium difficile infection following fecal microbiota transplantation. MBio 7, e01965-e01916. doi: 10.1128/mBio.01965-16
111. Suskind, D. L., Brittnacher, M. J., Wahbeh, G., Shaffer, M. L., Hayden, H. S., Qin, X., et al. (2015). Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn's disease. Inflamm. Bowel Dis. 21, 556-563. doi: 10.1097/MIB.0000000000000307
112. Takahashi, K., Nishida, A., Fujimoto, T., Fujii, M., Shioya, M., Imaeda, H., et al. (2016). Reduced abundance of butyrate-producing bacteria species in the fecal microbial community in Crohn's disease. Digestion 93, 59-65. doi: 10.1159/000441768
113. Tan, J., McKenzie, C., Potamitis, M., Thorburn, A. N., Mackay, C. R., and Macia, L. (2014). The role of short-chain fatty acids in health and disease. Adv. Immunol. 121:91-119. doi: 10.1016/B978-0-12-800100-4.00003-9
114. Thompson, S., Guetterman, H., Taylor, A., Bogner, A., Martin, D., Farrell, J. J., et al. (2016). Dietary predictors of fecal microbiota transplantation success. J. Acad. Nutr. Diet. 116:A76. doi: 10.1016/j.jand.2016.06.267
115. Thursby, E., and Juge, N. (2017). Introduction to the human gut microbiota. Biochem. J. 474, 1823-1836. doi: 10.1042/BCJ20160510
116. Tian, H., Ge, X., Nie, Y., Yang, L., Ding, C., McFarland, L.V., et al. (2017). Fecal microbiota transplantation in patients with slow-transit constipation: a randomized, clinical trial. PLoS ONE 12:e0171308. doi: 10.1371/journal.pone.0171308
117. van Nood, E., Vrieze, A., Nieuwdorp, M., Fuentes, S., Zoetendal, E. G., de Vos, W. M., et al. (2013). Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368, 407-415. doi: 10.1056/NEJMoa1205037
118. Vatanen, T., Kostic, A. D., d'Hennezel, E., Siljander, H., Franzosa, E.A., Yassour, M., et al. (2016). Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 165, 842-853. doi: 10.1016/j.cell.2016.04.007
119. Vaughn, B. P., Vatanen, T., Allegretti, J. R., Bai, A., Xavier, R. J., Korzenik, J., et al. (2016). Increased intestinal microbial diversity following fecal microbiota transplant for active Crohn's disease. Inflamm. Bowel Dis. 22, 2182-2190. doi: 10.1097/MIB.0000000000000893
120. Vermeire, S., Joossens, M., Verbeke, K., Wang, J., Machiels, K., Sabino, J., et al. (2016). Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohn's Colitis 10, 387-394. doi: 10.1093/ecco-jcc/jjv203
121. Vrieze, A., Van Nood, E., Holleman, F., Salojärvi, J., Kootte, R. S., Bartelsman, J. F., et al. (2012). Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913-916.e7. doi: 10.1053/j.gastro.2012.06.031
122. Walker, A. W., Sanderson, J. D., Churcher, C., Parkes, G. C., Hudspith, B. N., Rayment, N., et al. (2011). High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 11:7. doi: 10.1186/1471-2180-11-7
123. Wang, J., Thingholm, L. B., Skiecevičiene, J., Rausch, P., Kummen, M., Hov, J. R., et al. (2016). Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat. Genet. 48, 1396-1406. doi: 10.1038/ng.3695
124. Warny, M., Pepin, J., Fang, A., Killgore, G., Thompson, A., Brazier, J., et al. (2005). Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366, 1079-1084. doi: 10.1016/S0140-6736(05)67420-X
125. Weingarden, A., González, A., Vázquez-Baeza, Y., Weiss, S., Humphry, G., Berg-Lyons, D., et al. (2015). Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection. Microbiome 3:10. doi: 10.1186/s40168-
126. Willing, B. P., Dicksved, J., Halfvarson, J., Andersson, A. F., Lucio, M., Zheng, Z., et al. (2010). A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139, 1844-1854.e1. doi: 10.1053/j.gastro.2010.08.049
127. Xie, H., Guo, R., Zhong, H., Feng, Q., Lan, Z., Qin, B., et al. (2016). Shotgun metagenomics of 250 adult twins reveals genetic and environmental impacts on the gut microbiome. Cell Syst. 3, 572-584.e3. doi: 10.1016/j.cels.2016.10.004
128. Youngster, I., Russell, G. H., Pindar, C., Ziv-Baran, T., Sauk, J., and Hohmann, E. L. (2014). Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 312:1772. doi: 10.1001/jama.2014.13875
129. Zhang, F. M., Wang, H. G., Wang, M., Cui, B. T., Fan, Z. N., and Ji, G. Z. (2013). Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn's disease. World J. Gastroenterol. 19, 7213-7216. doi: 10.3748/wjg.v19.i41.7213
130. Zuo, T., Wong, S. H., Lam, K., Lui, R., Cheung, K., Tang, W., et al. (2018). Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut 67, 634-643. doi: 10.1136/gutjnl-2017-313952