Microbiota transplantation: concept, methodology and strategy for its modernization

Faming Zhang, Bota Cui, Xingxiang He, Yuqiang Nie, Kaichun Wu, Daiming Fan, FMT-standardization Study Group, Baisui Feng, Dongfeng Chen, Jianlin Ren, Mingming Deng, Ning Li, Pengyuan Zheng, Qing Cao, Shaoqi Yang, Xingxiang He, Yu Liu, Yuqiang Nie, Yongjian Zhou, Daiming Fan, Kaichun Wu, Yongzhan Nie, Guozhong Ji, Pan Li, Bota Cui, Faming Zhang, Faming Zhang, Bota Cui, Xingxiang He, Yuqiang Nie, Kaichun Wu, Daiming Fan, FMT-standardization Study Group, Baisui Feng, Dongfeng Chen, Jianlin Ren, Mingming Deng, Ning Li, Pengyuan Zheng, Qing Cao, Shaoqi Yang, Xingxiang He, Yu Liu, Yuqiang Nie, Yongjian Zhou, Daiming Fan, Kaichun Wu, Yongzhan Nie, Guozhong Ji, Pan Li, Bota Cui, Faming Zhang

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, gut-brain 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 step-up FMT strategy based on literature and state experts' perspectives.

Keywords: Clostridium difficile; bacteria; inflammatory bowel disease; microbiome; perspectives; selective microbiota transplantation; step-up fecal microbiota transplantation.

Figures

Figure 1
Figure 1
The changing of using microbial cells to treat human diseases
Figure 2
Figure 2
The delivering ways of microbiota transplantation in gastrointestinal tract
Figure 3
Figure 3
The step-up FMT strategy
Figure 4
Figure 4
The GMP laboratory for preparation of fecal microbiota

References

    1. Alang N, Kelly CR. Weight gain after fecal microbiota transplantation. Open Forum Infect Dis. 2015;2:ofv004.
    1. Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM. Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol. 2017;14:356–365.
    1. Andrews PJ, Borody TJ. “Putting back the bugs”: bacterial treatment relieves chronic constipation and symptoms of irritable bowel syndrome. Med J Aust. 1993;159:633–634.
    1. Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Kheradman R, Heuman D, Wang J, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. 2017;66:1727–1738.
    1. Bak SH, Choi HH, Lee J, Kim MH, Lee YH, Kim JS, Cho YS. Fecal microbiota transplantation for refractory Crohn’s disease. Intest Res. 2017;15:244–248.
    1. Baro E, Galperine T, Denies F, Lannoy D, Lenne X, Odou P, Guery B, Dervaux B. Cost-effectiveness analysis of five competing strategies for the management of multiple recurrent community-onset Clostridium difficile infection in France. PLOS ONE. 2017;12:e0170258.
    1. Baxter M, Ahmad T, Colville A, Sheridan R. Fatal aspiration pneumonia as a complication of fecal microbiota transplant. Clin Infect Dis. 2015;61:136–137.
    1. Bennet JD, Brinkman M. Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet. 1989;1:164.
    1. Borody TJ, George L, Andrews P, Brandl S, Noonan S, Cole P, Hyland L, Morgan A, Maysey J, Moore-Jones D. Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome. Med J Aust. 1989;150:604.
    1. Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, Stollman N, Rohlke F, Surawicz C. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107:1079–1087.
    1. Brodmann T, Endo A, Gueimonde M, Vinderola G, Kneifel W, de Vos WM, Salminen S, Gomez-Gallego C. Safety of novel microbes for human consumption: practical examples of assessment in the European Union. Front Microbiol. 2017;8:1725.
    1. Cammarota G, Ianiro G, Tilg H, Rajilic-Stojanovic M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66:569–580.
    1. Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23:314–326.
    1. Chu ND, Smith MB, Perrotta AR, Kassam Z, Alm EJ. Profiling living bacteria informs preparation of fecal microbiota transplantations. PLOS ONE. 2017;12:e0170922.
    1. Cui B, Zhang F. Fecal microbiota transplantation: understanding from holistic integrative view. AME Med J. 2018;3:1.
    1. Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Z, et al. Fecal microbiota transplantation through mid-gut for refractory Crohn’s disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol. 2015;30:51–58.
    1. Cui B, Li P, Xu L, Zhao Y, Wang H, Peng Z, Xu H, Xiang J, He Z, Zhang T, et al. Step-up fecal microbiota transplantation strategy: a pilot study for steroid-dependent ulcerative colitis. J Transl Med. 2015;13:298.
    1. Cui B, Li P, Xu L, Peng Z, Xiang J, He Z, Zhang T, Ji G, Nie Y, Wu K, et al. Step-up fecal microbiota transplantation (FMT) strategy. Gut Microbes. 2016;7:323–328.
    1. Cui M, Xiao H, Li Y, Zhou L, Zhao S, Luo D, Zheng Q, Dong J, Zhao Y, Zhang X, et al. Faecal microbiota transplantation protects against radiation-induced toxicity. EMBO Mol Med. 2017;9:448–461.
    1. Daillere R, Vetizou M, Waldschmitt N, Yamazaki T, Isnard C, Poirier-Colame V, Duong CP, Flament C, Lepage P, Roberti MP, et al. Enterococcus hirae and Barnesiella intestinihominis facilitate cyclophosphamide-induced therapeutic immunomodulatory effects. Immunity. 2016;45:931–943.
    1. Dubilier N, McFall-Ngai M, Zhao L. Microbiology: create a global microbiome effort. Nature. 2015;526:631–634.
    1. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44:854–859.
    1. Fan D. Holistic integrative medicine: toward a new era of medical advancement. Front Med. 2017;11:152–159.
    1. Ferreira MR, Muls A, Dearnaley DP, Andreyev HJ. Microbiota and radiation-induced bowel toxicity: lessons from inflammatory bowel disease for the radiation oncologist. Lancet Oncol. 2014;15:e139–e147.
    1. Fischer M, Sipe BW, Rogers NA, Cook GK, Robb BW, Vuppalanchi R, Rex DK. Faecal microbiota transplantation plus selected use of vancomycin for severe-complicated Clostridium difficile infection: description of a protocol with high success rate. Aliment Pharmacol Ther. 2015;42:470–476.
    1. Fischer M, Kao D, Kelly C, Kuchipudi A, Jafri SM, Blumenkehl M, Rex D, Mellow M, Kaur N, Sokol H, et al. Fecal microbiota transplantation is safe and efficacious for recurrent or refractory Clostridium difficile infection in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:2402–2409.
    1. Fischer M, Kao D, Mehta SR, Martin T, Dimitry J, Keshteli AH, Cook GK, Phelps E, Sipe BW, Xu H, et al. Predictors of early failure after fecal microbiota transplantation for the therapy of Clostridium difficile infection: a multicenter study. Am J Gastroenterol. 2016;111:1024–1031.
    1. Furuya-Kanamori L, Doi SA, Paterson DL, Helms SK, Yakob L, McKenzie SJ, Garborg K, Emanuelsson F, Stollman N, Kronman MP, et al. 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. 2017;51:145–150.
    1. Ge H. Zhou Hou Bei Ji Fang. Tianjin: Tianjin Science & Technology Press; 2000.
    1. Gibson MK, Pesesky MW, Dantas G. The yin and yang of bacterial resilience in the human gut microbiota. J Mol Biol. 2014;426:3866–3876.
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. 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. 2017;14:491–502.
    1. Goldenberg SD, Batra R, Batra R, Beales I, Digby-Bell JL, Irving PM, Kellingray L, Narbad A, Franslem-Elumogo N. Comparison of different strategies for providing fecal microbiota transplantation to treat patients with recurrent Clostridium difficile infection in two english hospitals: a review. Infect Dis Ther LID. 2018
    1. Gong J, Chehrazi-Raffle A, Reddi S, Salgia R. 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. 2018;6:8.
    1. Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science. 2018;359:97–103.
    1. Gweon TG, Kim J, Lim CH, Park JM, Lee DG, Lee IS, Cho YS, Kim SW, Choi MG. Fecal microbiota transplantation using upper gastrointestinal tract for the treatment of refractory or severe complicated Clostridium difficile infection in elderly patients in poor medical condition: the first study in an Asian country. Gastroenterol Res Pract. 2016;2016:2687605.
    1. Hale VL, Tan CL, Niu K, Yang Y, Cui D, Zhao H, Knight R, Amato KR. Effects of field conditions on fecal microbiota. J Microbiol Methods. 2016;130:180–188.
    1. Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A. Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107:761–767.
    1. He Z, Cui BT, Zhang T, Li P, Long CY, Ji GZ, Zhang FM. Fecal microbiota transplantation cured epilepsy in a case with Crohn’s disease: the first report. World J Gastroenterol. 2017;23:3565–3568.
    1. He Z, Li P, Zhu J, Cui B, Xu L, Xiang J, Zhang T, Long C, Huang G, Ji G, et al. Multiple fresh fecal microbiota transplants induces and maintains clinical remission in Crohn’s disease complicated with inflammatory mass. Sci Rep. 2017;7:4753.
    1. Hoffmann D, Palumbo F, Ravel J, Roghmann MC, Rowthorn V, von Rosenvinge E. Improving regulation of microbiota transplants. Science. 2017;358(80):1390–1391.
    1. Hoffmann DE, Palumbo FB, Ravel J, Rowthorn V, von Rosenvinge E. A proposed definition of microbiota transplantation for regulatory purposes. Gut Microbes. 2017;8:208–213.
    1. Jiang ZD, Ajami NJ, Petrosino JF, Jun G, Hanis CL, Shah M, Hochman L, Ankoma-Sey V, DuPont AW, Wong MC, et al. Randomised clinical trial: faecal microbiota transplantation for recurrent Clostridium difficile infection - fresh, or frozen, or lyophilised microbiota from a small pool of healthy donors delivered by colonoscopy. Aliment Pharmacol Ther. 2017;45:899–908.
    1. Johnsen PH, Hilpusch F, Cavanagh JP, Leikanger IS, Kolstad C, Valle PC, Goll R. 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. 2018;3:17–24.
    1. Kakihana K, Fujioka Y, Suda W, Najima Y, Kuwata G, Sasajima S, Mimura I, Morita H, Sugiyama D, Nishikawa H, et al. Fecal microbiota transplantation for patients with steroid-resistant acute graft-versus-host disease of the gut. Blood. 2016;128:2083–2088.
    1. Kang DW, Adams JB, Gregory AC, Borody T, Chittick L, Fasano A, Khoruts A, Geis E, Maldonado J, McDonough-Means S, et al. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome. 2017;5:10.
    1. Kao D, Roach B, Park H, Hotte N, Madsen K, Bain V, Tandon P. Fecal microbiota transplantation in the management of hepatic encephalopathy. Hepatology. 2016;63:339–340.
    1. Kellermayer R, Nagy-Szakal D, Harris RA, Luna RA, Pitashny M, Schady D, Mir SA, Lopez ME, Gilger MA, Belmont J, et al. Serial fecal microbiota transplantation alters mucosal gene expression in pediatric ulcerative colitis. Am J Gastroenterol. 2015;110:604–606.
    1. Kelly CR, Ihunnah C, Fischer M, Khoruts A, Surawicz C, Afzali A, Aroniadis O, Barto A, Borody T, Giovanelli A, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–1071.
    1. Kelly CR, Kahn S, Kashyap P, Laine L, Rubin D, Atreja A, Moore T, Wu G. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149:223–237.
    1. Kelly CR, Kim AM, Laine L, Wu GD. The AGA’s fecal microbiota transplantation national registry: an important step toward understanding risks and benefits of microbiota therapeutics. Gastroenterology. 2017;152:681–684.
    1. Khoruts A, Sadowsky MJ. Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol. 2016;13:508–516.
    1. Klatt NR, Cheu R, Birse K, Zevin AS, Perner M, Noel-Romas L, Grobler A, Westmacott G, Xie IY, et al. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science. 2017;356:938–945.
    1. Konijeti GG, Sauk J, Shrime MG, Gupta M, Ananthakrishnan AN. Cost-effectiveness of competing strategies for management of recurrent Clostridium difficile infection: a decision analysis. Clin Infect Dis. 2014;58:1507–1514.
    1. Lee CH, Belanger JE, Kassam Z, Smieja M, Higgins D, Broukhanski G, Kim PT. 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. 2014;33:1425–1428.
    1. Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D, Nematallah A, Weese JS, Collins S, Moayyedi P, Crowther M, et al. Frozen vs Fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. 2016;315:142–149.
    1. Li S. Ben Cao Gang Mu. Beijing: Huaxia Press; 2011.
    1. Liu SX, Li YH, Dai WK, Li XS, Qiu CZ, Ruan ML, Zou B, Dong C, Liu YH, He JY, et al. Fecal microbiota transplantation induces remission of infantile allergic colitis through gut microbiota re-establishment. World J Gastroenterol. 2017;23:8570–8581.
    1. Long C, Yu Y, Cui B, Jagessar AA, Zhang J, Ji G, Huang G, Zhang F. A novel quick transendoscopic enteral tubing in mid-gut: technique and training with video. BMC Gastroenterol. 2018;18:37.
    1. Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016;375:2369–2379.
    1. Ma Y, Liu J, Rhodes C, Nie Y, Zhang F. Ethical issues in fecal microbiota transplantation in practice. Am J Bioeth. 2017;17:34–45.
    1. Madsen JS, Sorensen SJ, Burmolle M. Bacterial social interactions and the emergence of community-intrinsic properties. Curr Opin Microbiol. 2017;42:104–109.
    1. Martz SL, Guzman-Rodriguez M, He SM, Noordhof C, Hurlbut DJ, Gloor GB, Carlucci C, Weese S, Allen-Vercoe E, Sun J, et al. A human gut ecosystem protects against C. difficile disease by targeting TcdA. J Gastroenterol. 2017;52:452–465.
    1. Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ, Gajewski TF. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 2018;359:104–108.
    1. Merlo G, Graves N, Brain D, Connelly LB. Economic evaluation of fecal microbiota transplantation for the treatment of recurrent Clostridium difficile infection in Australia. J Gastroenterol Hepatol. 2016;31:1927–1932.
    1. Miller LE, Zimmermann AK, Ouwehand AC. Contemporary meta-analysis of short-term probiotic consumption on gastrointestinal transit. World J Gastroenterol. 2016;22:5122–5131.
    1. Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149:102–109.e6.
    1. Ni X, Fan S, Zhang Y, Wang Z, Ding L, Li Y, Li J. Coordinated hospital-home fecal microbiota transplantation via percutaneous endoscopic cecostomy for recurrent steroid-dependent ulcerative colitis. Gut Liver. 2016;10:975–980.
    1. Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, Leong RW, Connor S, Ng W, Paramsothy R, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–1228.
    1. Peng Z, Xiang J, He Z, Zhang T, Xu L, Cui B, Li P, Huang G, Ji G, Nie Y, et al. Colonic transendoscopic enteral tubing: a novel way of transplanting fecal microbiota. Endosc Int Open. 2016;4:E610–E613.
    1. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, Brown EM, Schroeter K, Allen-Vercoe E. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome. 2013;1:3.
    1. Philips CA, Pande A, Shasthry SM, Jamwal KD, Khillan V, Chandel SS, Kumar G, Sharma MK, Maiwall R, Jindal A, et al. Healthy donor fecal microbiota transplantation in steroid-ineligible severe alcoholic hepatitis: a pilot study. Clin Gastroenterol Hepatol. 2017;15:600–602.
    1. Ren RR, Sun G, Yang YS, Peng LH, Wang SF, Shi XH, Zhao JQ, Ban YL, Pan F, Wang XH, et al. Chinese physicians’ perceptions of fecal microbiota transplantation. World J Gastroenterol. 2016;22:4757–4765.
    1. Ren YD, Ye ZS, Yang LZ, Jin LX, Wei WJ, Deng YY, Chen XX, Xiao CX, Yu XF, Xu HZ, et al. Fecal microbiota transplantation induces hepatitis B virus e-antigen (HBeAg) clearance in patients with positive HBeAg after long-term antiviral therapy. Hepatology. 2017;65:1765–1768.
    1. 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 WM, et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology. 2015;149(110–118):e4.
    1. Routy B, Le Chatelier E, Derosa L, Duong CPM, Alou MT, Daillère R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science. 2018;359:91–97.
    1. Schwartz JS, Peres AG, Mfuna EL, Cousineau B, Madrenas J, Desrosiers M. Topical probiotics as a therapeutic alternative for chronic rhinosinusitis: A preclinical proof of concept. Am J Rhinol Allergy. 2016;30:202–205.
    1. Seth AK, Rawal P, Bagga R, Jain P. Successful colonoscopic fecal microbiota transplantation for active ulcerative colitis: first report from India. Indian J Gastroenterol. 2016;35:393–395.
    1. Shimizu H, Arai K, Abe J, Nakabayashi K, Yoshioka T, Hosoi K, Kuroda M. Repeated fecal microbiota transplantation in a child with ulcerative colitis. Pediatr Int. 2016;58:781–785.
    1. Spindelboeck W, Schulz E, Uhl B, Kashofer K, Aigelsreiter A, Zinke-Cerwenka W, Mulabecirovic A, Kump PK, Halwachs B, Gorkiewicz G, et al. Repeated fecal microbiota transplantations attenuate diarrhea and lead to sustained changes in the fecal microbiota in acute, refractory gastrointestinal graft-versus-host-disease. Haematologica. 2017;102:e210–e213.
    1. Stallmach A, Anttila VJ, Hell M, Gwynn S, Merino-Amador P, Petrosillo N, Racil Z, Warren T, Wenisch C, Wilcox M. Inflammatory bowel disease and Clostridium difficile infection: contrasting views of international clinical professionals. Z Gastroenterol LID. 2018
    1. Starkel P, Leclercq S, de Timary P, Schnabl B. Intestinal dysbiosis and permeability: the yin and yang in alcohol dependence and alcoholic liver disease. Clin Sci (Lond) 2018;132:199–212.
    1. Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, McFarland LV, Mellow M, Zuckerbraun BS. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108:478–498.
    1. Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, Singh N, Damman CJ, Hager KR, Nielson H, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis. 2015;21:556–563.
    1. Tang G, Yin W, Liu W. 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. 2017;88:322–329.
    1. Tariq R, Pardi DS, Tosh PK, Walker RC, Razonable RR, Khanna S. Fecal microbiota transplantation for recurrent Clostridium difficile infection reduces recurrent urinary tract infection frequency. Clin Infect Dis. 2017;65:1745–1747.
    1. Tian H, Ding C, Gong J, Ge X, McFarland LV, Gu L, Wei Y, Chen Q, Zhu W, Li J, et al. Treatment of slow transit constipation with fecal microbiota transplantation: a pilot study. J Clin Gastroenterol. 2016;50:865–870.
    1. Uygun A, Ozturk K, Demirci H, Oger C, Avci IY, Turker T, Gulsen M. Fecal microbiota transplantation is a rescue treatment modality for refractory ulcerative colitis. Medicine (Baltimore) 2017;96:e6479.
    1. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–415.
    1. Varier RU, Biltaji E, Smith KJ, Roberts MS, Kyle JM, LaFleur J, Nelson RE. Cost-effectiveness analysis of fecal microbiota transplantation for recurrent Clostridium difficile infection. Infect Control Hosp Epidemiol. 2015;36:438–444.
    1. Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015;350:1079–1084.
    1. Vindigni SM, Surawicz CM. Fecal microbiota transplantation. Gastroenterol Clin North Am. 2017;46:171–185.
    1. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology. 2012;143:913–916.e7.
    1. Wang S, Xu M, Wang W, Cao X, Piao M, Khan S, Yan F, Cao H, Wang B. Systematic review: adverse events of fecal microbiota transplantation. PLOS ONE. 2016;11:e0161174.
    1. Waye A, Atkins K, Kao D. Cost averted with timely fecal microbiota transplantation in the management of recurrent Clostridium difficile infection in Alberta, Canada. J Clin Gastroenterol. 2016;50:747–753.
    1. Wei Y, Yang J, Wang J, Yang Y, Huang J, Gong H, Cui H, Chen D. Successful treatment with fecal microbiota transplantation in patients with multiple organ dysfunction syndrome and diarrhea following severe sepsis. Crit Care. 2016;20:332.
    1. Wong SH, Zhao L, Zhang X, Nakatsu G, Han J, Xu W, Xiao X, Kwong TN, Tsoi H, Wu WK, et al. Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice. Gastroenterology. 2017;153:1621–1633.e7.
    1. Wu W, Chen F, Liu Z, Cong Y. Microbiota-specific Th17 cells: Yin and Yang in regulation of inflammatory bowel disease. Inflamm Bowel Dis. 2016;22:1473–1482.
    1. Xu R. Chong Ding Tong Su Shang Han Lun. Beijing: China Press of Traditional Chinese Medicine; 2011.
    1. Xu L, Zhang T, Cui B, He Z, Xiang J, Long C, Peng Z, Li P, Huang G, Ji G, et al. Clinical efficacy maintains patients’ positive attitudes toward fecal microbiota transplantation. Medicine (Baltimore) 2016;95:e4055.
    1. Youngster I, Russell GH, Pindar C, Ziv-Baran T, Sauk J, Hohmann EL. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312:1772–1778.
    1. Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth N, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell. 2017;170(548–563):e16.
    1. Zhang F, Amateau SK, Khashab MA, Okolo PI., III Mid-gut stents. Curr Opin Gastroenterol. 2012;28:451–460.
    1. Zhang F, Luo W, Shi Y, Fan Z, Ji G. Should we standardize the 1,700-year-old fecal microbiota transplantation. Am J Gastroenterol. 2012;107:1755.
    1. Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ. Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn’s disease. World J Gastroenterol. 2013;19:7213–7216.
    1. Zhang T, Xiang J, Cui B, He Z, Li P, Chen H, Xu L, Ji G, Nie Y, Wu K, et al. Cost-effectiveness analysis of fecal microbiota transplantation for inflammatory bowel disease. Oncotarget. 2017;8:88894–88903.

Source: PubMed

3
購読する