|
|
|
Microbiota transplantation: concept, methodology and strategy for its modernization |
Faming Zhang1,2,3( ), Bota Cui1,2, Xingxiang He4, Yuqiang Nie5, Kaichun Wu6,7, Daiming Fan6,7, FMT-standardization Study Group |
1. Medical Center for Digestive Diseases, The Second Affiliated Hospital of Nanjing Medical University, Nanjing 210011, China 2. Key Lab of Holistic Integrative Enterology, Nanjing Medical University, Nanjing 211166, China 3. Division of Microbiotherapy, Sir Run Run Shaw Hospital, Nanjing Medical University, Nanjing 211166, China 4. Department of Gastroenterology, The First Affiliated Hospital of Guangdong Pharmaceutical University, Guangzhou 510080, China 5. Department of Gastroenterology, Guangzhou Digestive Disease Center, Guangzhou First People’s Hospital, Guangzhou Medical University, Guangzhou 510180, China 6. State Key Laboratory of Cancer Biology & Xijing Hospital of Digestive Diseases, Fourth Military Medical University, Xi’an 710032, China 7. National Clinical Research Center for Digestive Diseases, Xi’an 710032, China |
|
|
|
|
Abstract Fecal microbiota transplantation (FMT) has become a research focus of biomedicine and clinical medicine in recent years. The clinical response from FMT for different diseases provided evidence for microbiota-host interactions associated with various disorders, including Clostridium difficile infection, inflammatory bowel disease, diabetes mellitus, cancer, liver cirrhosis, gutbrain disease and others. To discuss the experiences of using microbes to treat human diseases from ancient China to current era should be important in moving standardized FMT forward and achieving a better future. Here, we review the changing concept of microbiota transplantation from FMT to selective microbiota transplantation, methodology development of FMT and stepup FMT strategy based on literature and state experts’ perspectives.
|
| Keywords
selective microbiota transplantation
microbiome
bacteria
Clostridium difficile
inflammatory bowel disease
step-up fecal microbiota transplantation
perspectives
|
|
Corresponding Author(s):
Faming Zhang
|
|
Issue Date: 08 June 2018
|
|
| 1 |
Alang N, Kelly CR (2015) Weight gain after fecal microbiota transplantation. Open Forum Infect Dis 2:ofv004
https://doi.org/10.1093/ofid/ofv004
|
| 2 |
Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM (2017) Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol 14:356–365
https://doi.org/10.1038/nrgastro.2017.20
|
| 3 |
Andrews PJ, Borody TJ (1993) “Putting back the bugs”: bacterial treatment relieves chronic constipation and symptoms of irritable bowel syndrome. Med J Aust 159:633–634
|
| 4 |
Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Kheradman R, Heuman D, Wang Jet al. (2017) Fecal microbiota transplant fromarational stooldonor improveshepaticencephalopathy: a randomized clinical trial. Hepatology 66:1727–1738
https://doi.org/10.1002/hep.29306
|
| 5 |
Bak SH, Choi HH, Lee J, Kim MH, Lee YH, Kim JS, Cho YS (2017) Fecal microbiota transplantation for refractory Crohn’s disease. Intest Res 15:244–248
https://doi.org/10.5217/ir.2017.15.2.244
|
| 6 |
Baro E, Galperine T, Denies F, Lannoy D, Lenne X, Odou P, Guery B, Dervaux B (2017) Cost-effectiveness analysis of five competing strategies for the management of multiple recurrent community-onset Clostridium difficile infection in France. PLOS ONE 12: e0170258
https://doi.org/10.1371/journal.pone.0170258
|
| 7 |
Baxter M, Ahmad T, Colville A, Sheridan R (2015) Fatal aspiration pneumonia as a complication of fecal microbiota transplant. Clin Infect Dis 61:136–137
https://doi.org/10.1093/cid/civ247
|
| 8 |
Bennet JD, Brinkman M (1989) Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet 1:164
https://doi.org/10.1016/S0140-6736(89)91183-5
|
| 9 |
Borody TJ, George L, Andrews P, Brandl S, Noonan S, Cole P, Hyland L, Morgan A, Maysey J,Moore-Jones D (1989) Bowelflora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome. Med J Aust 150:604
|
| 10 |
Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, Stollman N, Rohlke F, Surawicz C (2012) Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol 107:1079–1087
https://doi.org/10.1038/ajg.2012.60
|
| 11 |
Brodmann T, Endo A, Gueimonde M, Vinderola G, Kneifel W, de Vos WM, Salminen S, Gomez-Gallego C (2017) Safety of novel microbes for human consumption: practical examples of assessment in the European Union. Front Microbiol 8:1725
https://doi.org/10.3389/fmicb.2017.01725
|
| 12 |
Cammarota G, Ianiro G, Tilg H, Rajilic-Stojanovic M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart Aet al. (2017) European consensus conference on faecal microbiota transplantation in clinical practice. Gut 66:569–580
https://doi.org/10.1136/gutjnl-2016-313017
|
| 13 |
Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM (2017a) Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med 23:314–326
https://doi.org/10.1038/nm.4272
|
| 14 |
Chu ND, Smith MB, Perrotta AR, Kassam Z, Alm EJ (2017b) Profiling living bacteria informs preparation of fecal microbiota transplantations. PLOS ONE 12:e0170922
https://doi.org/10.1371/journal.pone.0170922
|
| 15 |
Cui B, Zhang F (2018) Fecal microbiota transplantation: understanding from holistic integrative view. AME Med J 3:1
https://doi.org/10.21037/amj.2017.11.13
|
| 16 |
Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Zet al. (2015a) Fecal microbiota transplantation through mid-gut for refractory Crohn’s disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol 30:51–58
https://doi.org/10.1111/jgh.12727
|
| 17 |
Cui B, Li P, Xu L, Zhao Y, Wang H, Peng Z, Xu H, Xiang J, He Z, Zhang Tet al.(2015b) Step-up fecal microbiota transplantation strategy: a pilot study for steroid-dependent ulcerative colitis . J Transl Med 13:298
https://doi.org/10.1186/s12967-015-0646-2
|
| 18 |
Cui B, Li P, Xu L, Peng Z, Xiang J, He Z, Zhang T, Ji G, Nie Y, Wu Ket al. (2016) Step-up fecal microbiota transplantation (FMT) strategy. Gut Microbes 7:323–328
https://doi.org/10.1080/19490976.2016.1151608
|
| 19 |
Cui M, Xiao H, Li Y, Zhou L, Zhao S, Luo D, Zheng Q, Dong J, Zhao Y, Zhang Xet al. (2017) Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol Med 9:448–461
https://doi.org/10.15252/emmm.201606932
|
| 20 |
Daillere R, Vetizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, Duong CP, Flament C, Lepage P, Roberti MPet al. (2016) Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity 45:931–943
https://doi.org/10.1016/j.immuni.2016.09.009
|
| 21 |
Dubilier N, McFall-Ngai M, Zhao L (2015) Microbiology: create a global microbiome effort. Nature 526:631–634
https://doi.org/10.1038/526631a
|
| 22 |
Eiseman B, Silen W, Bascom GS, Kauvar AJ (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44:854–859
|
| 23 |
Fan D (2017) Holistic integrative medicine: toward a new era of medical advancement. Front Med 11:152–159
https://doi.org/10.1007/s11684-017-0499-6
|
| 24 |
Ferreira MR, Muls A, Dearnaley DP, Andreyev HJ (2014) Microbiota and radiation-induced bowel toxicity: lessons from inflammatory bowel disease for the radiation oncologist. Lancet Oncol 15: e139–e147
https://doi.org/10.1016/S1470-2045(13)70504-7
|
| 25 |
Fischer M, Sipe BW, Rogers NA, Cook GK, Robb BW, Vuppalanchi R, Rex DK (2015) Faecal microbiota transplantation plus selected use of vancomycin for severe-complicated Clostridium difficileinfection: description of a protocol with high success rate. Aliment Pharmacol Ther 42:470–476
https://doi.org/10.1111/apt.13290
|
| 26 |
Fischer M, Kao D, Kelly C, Kuchipudi A, Jafri SM, Blumenkehl M, Rex D,Mellow M,Kaur N , Sokol Het al. (2016a) Fecal microbiota transplantation is safe and efficacious for recurrent or refractory Clostridium difficileinfection in patients with inflammatory bowel disease. Inflamm Bowel Dis 22:2402–2409
https://doi.org/10.1097/MIB.0000000000000908
|
| 27 |
Fischer M, Kao D, Mehta SR, Martin T, Dimitry J, Keshteli AH, Cook GK, Phelps E, Sipe BW, Xu Het al. (2016b) Predictors of early failure after fecal microbiota transplantation for the therapy of Clostridium difficileinfection: a multicenter study. Am J Gastroenterol 111:1024–1031
https://doi.org/10.1038/ajg.2016.180
|
| 28 |
Furuya-Kanamori L, Doi SA, Paterson DL, Helms SK, Yakob L, McKenzie SJ, Garborg K, Emanuelsson F,Stollman N, Kronman MPet al. (2017) Upper versus lower gastrointestinal delivery for transplantation of fecal microbiota in recurrent or refractory Clostridium difficile infection: a collaborative analysis of individual patient data from 14 studies. J Clin Gastroenterol 51:145–150
https://doi.org/10.1097/MCG.0000000000000511
|
| 29 |
Ge H (2000) Zhou Hou Bei Ji Fang. Tianjin Science & Technology Press, Tianjin
|
| 30 |
Gibson MK, Pesesky MW, Dantas G (2014) The yin and yang of bacterial resilience in the human gut microbiota. J Mol Biol 426:3866–3876
https://doi.org/10.1016/j.jmb.2014.05.029
|
| 31 |
Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PDet al. (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502
https://doi.org/10.1038/nrgastro.2017.75
|
| 32 |
Goldenberg SD, Batra R,Batra R, Beales I, Digby-Bell JL, Irving PM, Kellingray L, Narbad A, Franslem-Elumogo N (2018) Comparison of different strategies for providing fecal microbiota transplantation to treat patients with recurrent Clostridium difficileinfection in two english hospitals: a review. Infect Dis Ther LID.
https://doi.org/10.1007/s40121-018-0189-y
|
| 33 |
Gong J, Chehrazi-Raffle A, Reddi S, Salgia R (2018) Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: a comprehensive review of registration trials and future considerations. J Immunother Cancer 6:8
https://doi.org/10.1186/s40425-018-0316-z
|
| 34 |
Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SCet al. (2018) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359:97–103
https://doi.org/10.1126/science.aan4236
|
| 35 |
Gweon TG, Kim J, Lim CH, Park JM, Lee DG, Lee IS, Cho YS, Kim SW, Choi MG (2016) Fecal microbiota transplantation using upper gastrointestinal tract for the treatment of refractory or severe complicated Clostridium difficileinfection in elderly patients in poor medical condition: the first study in an Asian country. Gastroenterol Res Pract 2016:2687605
https://doi.org/10.1155/2016/2687605
|
| 36 |
Hale VL, Tan CL, Niu K, Yang Y, Cui D, Zhao H, Knight R, Amato KR (2016) Effects of field conditions on fecal microbiota. J Microbiol Methods 130:180–188
https://doi.org/10.1016/j.mimet.2016.09.017
|
| 37 |
Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A (2012) Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficileinfection. Am J Gastroenterol 107:761–767
https://doi.org/10.1038/ajg.2011.482
|
| 38 |
He Z, Cui BT, Zhang T, Li P, Long CY, Ji GZ, Zhang FM (2017a) Fecal microbiota transplantation cured epilepsy in a case with Crohn’s disease: the first report. World J Gastroenterol 23:3565–3568
https://doi.org/10.3748/wjg.v23.i19.3565
|
| 39 |
He Z, Li P,Zhu J, Cui B, Xu L, Xiang J, Zhang T, Long C, Huang G, Ji Get al. (2017b) Multiple fresh fecal microbiota transplants induces and maintains clinical remission in Crohn’s disease complicated with inflammatory mass. Sci Rep 7:4753
https://doi.org/10.1038/s41598-017-04984-z
|
| 40 |
Hoffmann D, Palumbo F, Ravel J, Roghmann MC, Rowthorn V, von Rosenvinge E (2017a) Improving regulation of microbiota transplants. Science 358(80):1390–1391
https://doi.org/10.1126/science.aaq0034
|
| 41 |
Hoffmann DE, Palumbo FB, Ravel J, Rowthorn V, von Rosenvinge E (2017b) A proposed definition of microbiota transplantation for regulatory purposes. Gut Microbes 8:208–213
https://doi.org/10.1080/19490976.2017.1293223
|
| 42 |
Jiang ZD, Ajami NJ, Petrosino JF, Jun G, Hanis CL, Shah M, Hochman L, Ankoma-Sey V, DuPont AW, Wong MCet al. (2017) Randomised clinical trial: faecal microbiota transplantation for recurrent Clostridium difficileinfection- fresh, or frozen, or lyophilised microbiota from a small pool of healthy donors delivered by colonoscopy. Aliment Pharmacol Ther 45:899–908
https://doi.org/10.1111/apt.13969
|
| 43 |
Johnsen PH, Hilpusch F, Cavanagh JP, Leikanger IS, Kolstad C, Valle PC, Goll R (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
https://doi.org/10.1016/S2468-1253(17)30338-2
|
| 44 |
Kakihana K, Fujioka Y, Suda W, Najima Y, Kuwata G, Sasajima S, Mimura I, Morita H, Sugiyama D, Nishikawa Het al. (2016) Fecal microbiota transplantation for patients with steroid-resistant acute graft-versus-host disease of the gut. Blood 128:2083–2088
https://doi.org/10.1182/blood-2016-05-717652
|
| 45 |
Kang DW, Adams JB, Gregory AC, Borody T, Chittick L, Fasano A, Khoruts A, Geis E, Maldonado J, McDonough-Means Set al. (2017) Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5:10
https://doi.org/10.1186/s40168-016-0225-7
|
| 46 |
Kao D, Roach B, Park H, Hotte N, Madsen K, Bain V,Tandon P (2016) Fecal microbiota transplantation in the management of hepatic encephalopathy. Hepatology 63:339–340
https://doi.org/10.1002/hep.28121
|
| 47 |
Kellermayer R, Nagy-Szakal D, Harris RA, Luna RA, Pitashny M, Schady D, Mir SA, Lopez ME, Gilger MA, Belmont Jet al. (2015) Serial fecal microbiota transplantation alters mucosal gene expression in pediatric ulcerative colitis. Am J Gastroenterol 110:604–606
https://doi.org/10.1038/ajg.2015.19
|
| 48 |
Kelly CR, Ihunnah C, Fischer M, Khoruts A, Surawicz C, Afzali A, Aroniadis O, Barto A, Borody T, Giovanelli Aet al. (2014) Fecal microbiota transplant for treatment of Clostridium difficileinfection in immunocompromised patients. Am J Gastroenterol 109:1065–1071
https://doi.org/10.1038/ajg.2014.133
|
| 49 |
Kelly CR, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T, Wu G (2015) Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology 149:223–237
https://doi.org/10.1053/j.gastro.2015.05.008
|
| 50 |
Kelly CR, Kim AM, Laine L, Wu GD (2017) The AGA’s fecal microbiota transplantation national registry: an important step toward understanding risks and benefits of microbiota therapeutics. Gastroenterology 152:681–684
https://doi.org/10.1053/j.gastro.2017.01.028
|
| 51 |
Khoruts A, Sadowsky MJ (2016) Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol 13:508–516
https://doi.org/10.1038/nrgastro.2016.98
|
| 52 |
Klatt NR, Cheu R, Birse K, Zevin AS, Perner M, Noel-Romas L, Grobler A, Westmacott G, Xie IYet al.(2017) Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science 356:938–945
https://doi.org/10.1126/science.aai9383
|
| 53 |
Konijeti GG, Sauk J, Shrime MG, Gupta M, Ananthakrishnan AN (2014) Cost-effectiveness of competing strategies for management of recurrent Clostridium difficileinfection: a decision analysis. Clin Infect Dis 58:1507–1514
https://doi.org/10.1093/cid/ciu128
|
| 54 |
Lee CH, Belanger JE, Kassam Z, Smieja M, Higgins D, Broukhanski G, Kim PT (2014) The outcome and long-term follow-up of 94 patients with recurrent and refractory Clostridium difficileinfection using single to multiple fecal microbiota transplantation via retention enema. Eur J Clin Microbiol Infect Dis 33:1425–1428
https://doi.org/10.1007/s10096-014-2088-9
|
| 55 |
Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D, Nematallah A, Weese JS, Collins S, Moayyedi P, Crowther Met al. (2016) Frozen vs Fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficileinfection: a randomized clinical trial. JAMA 315:142–149
https://doi.org/10.1001/jama.2015.18098
|
| 56 |
Li S (2011) Ben Cao Gang Mu. Huaxia Press, Beijing
|
| 57 |
Liu SX, Li YH, Dai WK, Li XS, Qiu CZ, Ruan ML, Zou B, Dong C, Liu YH, He JYet al. (2017) Fecal microbiota transplantation induces remission of infantile allergic colitis through gut microbiota reestablishment. World J Gastroenterol 23:8570–8581
https://doi.org/10.3748/wjg.v23.i48.8570
|
| 58 |
Long C, Yu Y, Cui B, Jagessar AA, Zhang J, Ji G, Huang G, Zhang F (2018) A novel quick transendoscopic enteral tubing in mid-gut: technique and training with video. BMC Gastroenterol 18:37
https://doi.org/10.1186/s12876-018-0766-2
|
| 59 |
Lynch SV, Pedersen O (2016) The human intestinal microbiome in health and disease. N Engl J Med 375:2369–2379
https://doi.org/10.1056/NEJMra1600266
|
| 60 |
Ma Y, Liu J, Rhodes C, Nie Y, Zhang F (2017) Ethical issues in fecal microbiota transplantation in practice. Am J Bioeth 17:34–45
https://doi.org/10.1080/15265161.2017.1299240
|
| 61 |
Madsen JS, Sorensen SJ, Burmolle M (2017) Bacterial social interactions and the emergence of community-intrinsic properties. Curr Opin Microbiol 42:104–109
https://doi.org/10.1016/j.mib.2017.11.018
|
| 62 |
Martz SL, Guzman-Rodriguez M, He SM, Noordhof C, Hurlbut DJ, Gloor GB, Carlucci C, Weese S, Allen-Vercoe E,Sun Jet al. (2017) A human gut ecosystem protects against C. difficile disease by targeting TcdA. J Gastroenterol 52:452–465
https://doi.org/10.1007/s00535-016-1232-y
|
| 63 |
Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF (2018) The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359:104–108
https://doi.org/10.1126/science.aao3290
|
| 64 |
Merlo G, Graves N, Brain D, Connelly LB (2016) Economic evaluation of fecal microbiota transplantation for the treatment of recurrent Clostridium difficileinfection in Australia. J Gastroenterol Hepatol 31:1927–1932
https://doi.org/10.1111/jgh.13402
|
| 65 |
Miller LE, Zimmermann AK, Ouwehand AC (2016) Contemporary meta-analysis of short-term probiotic consumption on gastrointestinal transit. World J Gastroenterol 22:5122–5131
https://doi.org/10.3748/wjg.v22.i21.5122
|
| 66 |
Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch Wet al. (2015) Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149:102–109.e6
https://doi.org/10.1053/j.gastro.2015.04.001
|
| 67 |
Ni X, Fan S, Zhang Y, Wang Z, Ding L, Li Y, Li J (2016) Coordinated hospital-home fecal microbiota transplantation via percutaneous endoscopic cecostomy for recurrent steroid-dependent ulcerative colitis. Gut Liver 10:975–980
https://doi.org/10.5009/gnl15456
|
| 68 |
Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J,Samuel D, Leong RW, Connor S, Ng W, Paramsothy Ret al. (2017) Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet 389:1218–1228
https://doi.org/10.1016/S0140-6736(17)30182-4
|
| 69 |
Peng Z, Xiang J, He Z, Zhang T, Xu L, Cui B, Li P, Huang G, Ji G, Nie Yet al. (2016) Colonic transendoscopic enteral tubing: a novel way of transplanting fecal microbiota. Endosc Int Open 4:E610–E613
https://doi.org/10.1055/s-0042-105205
|
| 70 |
Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, Brown EM, Schroeter K, Allen-Vercoe E (2013) Stool substitute transplant therapy for the eradication of Clostridium difficileinfection: ‘RePOOPulating’ the gut. Microbiome 1:3
https://doi.org/10.1186/2049-2618-1-3
|
| 71 |
Philips CA, Pande A, Shasthry SM, Jamwal KD, Khillan V,Chandel SS, Kumar G, Sharma MK, Maiwall R, Jindal Aet al. (2017) Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin Gastroenterol Hepatol 15:600–602
https://doi.org/10.1016/j.cgh.2016.10.029
|
| 72 |
Ren RR, Sun G, Yang YS, Peng LH, Wang SF, Shi XH, Zhao JQ, Ban YL, Pan F, Wang XHet al. (2016) Chinese physicians’ perceptions of fecal microbiota transplantation. World J Gastroenterol 22:4757–4765
https://doi.org/10.3748/wjg.v22.i19.4757
|
| 73 |
Ren YD, Ye ZS, Yang LZ, Jin LX, Wei WJ, Deng YY, Chen XX, Xiao CX, Yu XF, Xu HZet 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
https://doi.org/10.1002/hep.29008
|
| 74 |
Rossen NG, Fuentes S, van der Spek MJ, Tijssen JG, Hartman JH, Duflou A, Lowenberg M, van den Brink GR, Mathus-Vliegen EM, de Vos WMet al. (2015) Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 149(110–118):e4
|
| 75 |
Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C,Roberti MP (2018) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359:91–97
https://doi.org/10.1126/science.aan3706
|
| 76 |
Schwartz JS, Peres AG, Mfuna EL, Cousineau B, Madrenas J, Desrosiers M (2016) Topical probiotics as a therapeutic alternative for chronic rhinosinusitis: A preclinical proof of concept. Am J Rhinol Allergy 30:202–205
https://doi.org/10.2500/ajra.2016.30.4372
|
| 77 |
Seth AK, Rawal P, Bagga R, Jain P (2016) Successful colonoscopic fecal microbiota transplantation for active ulcerative colitis: first report from India. Indian J Gastroenterol 35:393–395
https://doi.org/10.1007/s12664-016-0696-2
|
| 78 |
Shimizu H, Arai K, Abe J,Nakabayashi K, Yoshioka T, Hosoi K, Kuroda M (2016) Repeated fecal microbiota transplantation in a child with ulcerative colitis. Pediatr Int 58:781–785
https://doi.org/10.1111/ped.12967
|
| 79 |
Spindelboeck W, Schulz E, Uhl B, Kashofer K, Aigelsreiter A, Zinke-Cerwenka W, Mulabecirovic A, Kump PK, Halwachs B, Gorkiewicz Get al. (2017) Repeated fecal microbiota transplantations attenuate diarrhea and lead to sustained changes in the fecal microbiota in acute, refractory gastrointestinal graft-versus-hostdisease. Haematologica 102:e210–e213
https://doi.org/10.3324/haematol.2016.154351
|
| 80 |
Stallmach A, Anttila VJ, Hell M, Gwynn S, Merino-Amador P, Petrosillo N, Racil Z, Warren T, Wenisch C, Wilcox M (2018) Inflammatory bowel disease and Clostridium difficile infection: contrasting views of international clinical professionals. Z Gastroenterol LID.
https://doi.org/10.1055/s-0044-100045
|
| 81 |
Starkel P, Leclercq S, de Timary P, Schnabl B (2018) Intestinal dysbiosis and permeability: the yin and yang in alcohol dependence and alcoholic liver disease. Clin Sci (Lond) 132:199–212
https://doi.org/10.1042/CS20171055
|
| 82 |
Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, McFarland LV, Mellow M, Zuckerbraun BS (2013) Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 108:478–498 (quiz 499)
|
| 83 |
Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, Singh N, Damman CJ, Hager KR, Nielson Het al. (2015) Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis 21:556–563
https://doi.org/10.1097/MIB.0000000000000307
|
| 84 |
Tang G, Yin W, Liu W (2017) Is frozen fecal microbiota transplantation as effective as fresh fecal microbiota transplantation in patients with recurrent or refractory Clostridium difficile infection: a meta-analysis. Diagn Microbiol Infect Dis 88:322–329
https://doi.org/10.1016/j.diagmicrobio.2017.05.007
|
| 85 |
Tariq R, Pardi DS, Tosh PK, Walker RC, Razonable RR, Khanna S (2017) Fecal microbiota transplantation for recurrent Clostridium difficile infection reduces recurrent urinary tract infection frequency. Clin Infect Dis 65:1745–1747
https://doi.org/10.1093/cid/cix618
|
| 86 |
Tian H, Ding C, Gong J, Ge X, McFarland LV, Gu L, Wei Y, Chen Q, ZhuW, Li Jet al. (2016) Treatment of slow transit constipation with fecal microbiota transplantation: a pilot study. J Clin Gastroenterol 50:865–870
https://doi.org/10.1097/MCG.0000000000000472
|
| 87 |
Uygun A, Ozturk K, Demirci H,Oger C,Avci IY, Turker T,Gulsen M(2017) Fecal microbiota transplantation is a rescue treatment modality for refractory ulcerative colitis. Medicine (Baltimore) 96:e6479
https://doi.org/10.1097/MD.0000000000006479
|
| 88 |
van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JGet al. (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368:407–415
https://doi.org/10.1056/NEJMoa1205037
|
| 89 |
Varier RU, Biltaji E, Smith KJ, Roberts MS, Kyle JM, LaFleur J, Nelson RE (2015) Cost-effectiveness analysis of fecal microbiota transplantation for recurrent Clostridium difficile infection. Infect Control Hosp Epidemiol 36:438–444
https://doi.org/10.1017/ice.2014.80
|
| 90 |
Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPet al. (2015) Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350:1079–1084
https://doi.org/10.1126/science.aad1329
|
| 91 |
Vindigni SM, Surawicz CM (2017) Fecal microbiota transplantation. Gastroenterol Clin North Am 46:171–185
https://doi.org/10.1016/j.gtc.2016.09.012
|
| 92 |
Vrieze A, Van Nood E, Holleman F, Salojarvi J,Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer Ret al. (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143:913–916.e7
https://doi.org/10.1053/j.gastro.2012.06.031
|
| 93 |
Wang S, Xu M, Wang W, Cao X, Piao M, Khan S, Yan F, Cao H, Wang B (2016) Systematic review: adverse events of fecal microbiota transplantation. PLOS ONE 11:e0161174
https://doi.org/10.1371/journal.pone.0161174
|
| 94 |
Waye A, Atkins K, Kao D (2016) Cost averted with timely fecal microbiota transplantation in the management of recurrent Clostridium difficile infection in Alberta, Canada. J Clin Gastroenterol 50:747–753
https://doi.org/10.1097/MCG.0000000000000494
|
| 95 |
Wei Y, Yang J, Wang J,Yang Y, Huang J, Gong H, Cui H, Chen D (2016) Successful treatment with fecal microbiota transplantation in patients with multiple organ dysfunction syndrome and diarrhea following severe sepsis. Crit Care 20:332
https://doi.org/10.1186/s13054-016-1491-2
|
| 96 |
Wong SH, Zhao L, Zhang X, Nakatsu G,Han J, Xu W, Xiao X, Kwong TN, Tsoi H, Wu WKet al. (2017) Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology 153:1621–1633.e7
https://doi.org/10.1053/j.gastro.2017.08.022
|
| 97 |
Wu W, Chen F, Liu Z, Cong Y (2016) Microbiota-specific Th17 cells: Yin and Yang in regulation of inflammatory bowel disease. Inflamm Bowel Dis 22:1473–1482
https://doi.org/10.1097/MIB.0000000000000775
|
| 98 |
Xu R (2011) Chong Ding Tong Su Shang Han Lun. China Press of Traditional Chinese Medicine, Beijing
|
| 99 |
Xu L, Zhang T, Cui B, He Z, Xiang J, Long C, Peng Z, Li P, Huang G, Ji Get al. (2016) Clinical efficacy maintains patients’ positive attitudes toward fecal microbiota transplantation. Medicine (Baltimore) 95:e4055
https://doi.org/10.1097/MD.0000000000004055
|
| 100 |
Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL (2014) Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA 312:1772–1778
https://doi.org/10.1001/jama.2014.13875
|
| 101 |
Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth Net al. (2017) Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 170(548–563):e16
https://doi.org/10.1016/j.cell.2017.07.008
|
| 102 |
Zhang F,Amateau SK, Khashab MA, Okolo PI III (2012a) Mid-gut stents. Curr Opin Gastroenterol 28:451–460
https://doi.org/10.1097/MOG.0b013e3283561f3b
|
| 103 |
Zhang F, Luo W, Shi Y, Fan Z, Ji G (2012b) Should we standardize the 1,700-year-old fecal microbiota transplantation. Am J Gastroenterol 107:1755 (author reply p. 1755-1756)
|
| 104 |
Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ (2013) Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn’s disease. World J Gastroenterol 19:7213–7216
https://doi.org/10.3748/wjg.v19.i41.7213
|
| 105 |
Zhang T,Xiang J, Cui B, He Z, Li P, Chen H, Xu L, Ji G, Nie Y, Wu Ket al. (2017) Cost-effectiveness analysis of fecal microbiota transplantation for inflammatory bowel disease. Oncotarget 8:88894–88903
https://doi.org/10.18632/oncotarget.21491
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|