6,160
Views
13
CrossRef citations to date
0
Altmetric
Research Paper

The interplay of gut microbiota between donors and recipients determines the efficacy of fecal microbiota transplantation

, , , , & ORCID Icon
Article: 2100197 | Received 20 Nov 2021, Accepted 01 Jul 2022, Published online: 19 Jul 2022

References

  • Lessa FC, Mu Y, Bamberg WM, Beldavs ZG, Dumyati GK, Dunn JR, Farley MM, Holzbauer SM, Meek JI, Phipps EC, et al. Burden of clostridium difficile infection in the United States. N Engl J Med. 2015;372(9):825–20. doi:10.1056/NEJMoa1408913.
  • Alatab S, Sepanlou SG, Ikuta K, Vahedi H, Bisignano C, Safiri S, Sadeghi A, Nixon MR, Abdoli A, Abolhassani H, et al. The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5(1):17–30. doi:10.1016/S2468-1253(19)30333-4.
  • Goodhand JR, Alazawi W, Rampton D. Systematic review: clostridium difficile and IBD. Gut. 2011;60(Suppl 1):A146–A146. doi:10.1136/gut.2011.239301.309.
  • Chandra H, Sharma KK, Tuovinen OH, Sun X, Shukla P. Pathobionts: mechanisms of survival, expansion, and interaction with host with a focus on Clostridioides difficile. Gut Microbes. 2021;13(1):1979882. doi:10.1080/19490976.2021.1979882.
  • Ahlawat S, Kumar P, Mohan H, Goyal S, Sharma KK. Inflammatory bowel disease: tri-directional relationship between microbiota, immune system and intestinal epithelium. Crit Rev Microbiol. 2021;47(2):254–273. doi:10.1080/1040841X.2021.1876631.
  • Nitzan O, Elias M, Chazan B, Raz R, Saliba W. Clostridium difficile and inflammatory bowel disease: role in pathogenesis and implications in treatment. World J Gastroenterol. 2013;19(43):7577–7585. doi:10.3748/wjg.v19.i43.7577.
  • Rodriguez C, Romero E, Garrido-Sanchez L, Alcaín-Martínez G, Andrade RJ, Taminiau B, Daube G, García-Fuentes E. Microbiota insights in clostridium difficile infection and inflammatory bowel disease. Gut Microbes. 2020;12(1):1725220. doi:10.1080/19490976.2020.1725220.
  • Kelly CP. Fecal microbiota transplantation–an old therapy comes of age. N Engl J Med. 2013;368(5):474–475. doi:10.1056/NEJMe1214816.
  • Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, Leong RWL, 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(10075):1218–1228. doi:10.1016/S0140-6736(17)30182-4.
  • Halkjaer SI, Christensen AH, Lo BZS, Browne PD, Günther S, Hansen LH, Petersen AM. Faecal microbiota transplantation alters gut microbiota in patients with irritable bowel syndrome: results from a randomised, double-blind placebo-controlled study. Gut. 2018;67(12):2107–2115. doi:10.1136/gutjnl-2018-316434.
  • van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med. 2013;368(5):407–415. doi:10.1056/NEJMoa1205037.
  • Colman RJ, Rubin DT. Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis. 2014;8(12):1569–1581. doi:10.1016/j.crohns.2014.08.006.
  • Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, Ferrante M, Van Assche G, Rutgeerts P, Raes J, et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohns Colitis. 2016;10(4):387–394. doi:10.1093/ecco-jcc/jjv203.
  • Wilson BC, Vatanen T, Cutfield WS, O’Sullivan JM. The super-donor phenomenon in fecal microbiota transplantation. Front Cell Infect Microbiol. 2019;9:2. doi:10.3389/fcimb.2019.00002.
  • Xiao Y, Angulo MT, Lao S, Weiss ST, Liu -Y-Y. An ecological framework to understand the efficacy of fecal microbiota transplantation. Nat Commun. 2020;11(1):3329. doi:10.1038/s41467-020-17180-x.
  • Danne C, Rolhion N, Sokol H. Recipient factors in faecal microbiota transplantation: one stool does not fit all. Nat Rev Gastroenterol Hepatol. 2021;18(7):503–513. doi:10.1038/s41575-021-00441-5.
  • Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes. 2013;4(2):125–135. doi:10.4161/gmic.23571.
  • Li SS, Zhu A, Benes V, Costea PI, Hercog R, Hildebrand F, Huerta-Cepas J, Nieuwdorp M, Salojärvi J, Voigt AY, et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science. 2016;352(6285):586–589. doi:10.1126/science.aad8852.
  • Smillie CS, Sauk J, Gevers D, Friedman J, Sung J, Youngster I, Hohmann EL, Staley C, Khoruts A, Sadowsky MJ, et al. Strain tracking reveals the determinants of bacterial engraftment in the human gut following fecal microbiota transplantation. Cell Host Microbe. 2018;23(2):229–240 e5. doi:10.1016/j.chom.2018.01.003.
  • Goyal A, Yeh A, Bush BR, Firek BA, Siebold LM, Rogers MB, Kufen AD, Morowitz MJ. Safety, clinical response, and microbiome findings following fecal microbiota transplant in children with inflammatory bowel disease. Inflamm Bowel Dis. 2018;24(2):410–421. doi:10.1093/ibd/izx035.
  • Li P, Zhang T, Xiao Y, Tian L, Cui B, Ji G, Liu -Y-Y, Zhang F. Timing for the second fecal microbiota transplantation to maintain the long-term benefit from the first treatment for Crohn’s disease. Appl Microbiol Biotechnol. 2019;103(1):349–360. doi:10.1007/s00253-018-9447-x.
  • Mintz M, Khair S, Grewal S, LaComb JF, Park J, Channer B, Rajapakse R, Bucobo JC, Buscaglia JM, Monzur F, et al. Longitudinal microbiome analysis of single donor fecal microbiota transplantation in patients with recurrent Clostridium difficile infection and/or ulcerative colitis. PLoS One. 2018;13(1):e0190997. doi:10.1371/journal.pone.0190997.
  • Khanna S, Vazquez-Baeza Y, González A, Weiss S, Schmidt B, Muñiz-Pedrogo DA, Rainey JF, Kammer P, Nelson H, Sadowsky M, et al. Changes in microbial ecology after fecal microbiota transplantation for recurrent C. difficile infection affected by underlying inflammatory bowel disease. Microbiome. 2017;5(1):55. doi:10.1186/s40168-017-0269-3.
  • Weingarden A, González A, Vázquez-Baeza Y, Weiss S, Humphry G, Berg-Lyons D, Knights D, Unno T, Bobr A, Kang J, et al. Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection. Microbiome. 2015;3:10. doi:10.1186/s40168-015-0070-0.
  • Seekatz AM, Aas J, Gessert CE, Rubin TA, Saman DM, Bakken JS, Young VB. Recovery of the gut microbiome following fecal microbiota transplantation. mBio. 2014;5(3):e00893–14. doi:10.1128/mBio.00893-14.
  • Shankar V, Hamilton MJ, Khoruts A, Kilburn A, Unno T, Paliy O, Sadowsky MJ. Species and genus level resolution analysis of gut microbiota in Clostridium difficile patients following fecal microbiota transplantation. Microbiome. 2014;2(13):13. doi:10.1186/2049-2618-2-13.
  • Staley C, Vaughn BP, Graiziger CT, Singroy S, Hamilton MJ, Yao D, Chen C, Khoruts A, Sadowsky MJ. Community dynamics drive punctuated engraftment of the fecal microbiome following transplantation using freeze-dried, encapsulated fecal microbiota. Gut Microbes. 2017;8(3):276–288. doi:10.1080/19490976.2017.1299310.
  • Kelly CR, Khoruts A, Staley C, Sadowsky MJ, Abd M, Alani M, Bakow B, Curran P, McKenney J, Tisch A, et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent clostridium difficile infection. Ann Intern Med. 2016;165(9):609–616. doi:10.7326/M16-0271.
  • Zuo T, Wong SH, Lam K, Lui R, Cheung K, Tang W, Ching JYL, Chan PKS, Chan MCW, Wu JCY, et al. Bacteriophage transfer during faecal microbiota transplantation in Clostridium difficile infection is associated with treatment outcome. Gut. 2018;67(4):634–643. doi:10.1136/gutjnl-2017-313952.
  • Seekatz AM, Theriot CM, Rao K, Chang Y-M, Freeman AE, Kao JY, Young VB. Restoration of short chain fatty acid and bile acid metabolism following fecal microbiota transplantation in patients with recurrent Clostridium difficile infection. Anaerobe. 2018;53:64–73. doi:10.1016/j.anaerobe.2018.04.001.
  • Camacho-Ortiz A, Gutiérrez-Delgado EM, Garcia-Mazcorro JF, Mendoza-Olazarán S, Martínez-Meléndez A, Palau-Davila L, Baines SD, Maldonado-Garza H, Garza-González E. Randomized clinical trial to evaluate the effect of fecal microbiota transplant for initial Clostridium difficile infection in intestinal microbiome. PLoS One. 2017;12(12):e0189768. doi:10.1371/journal.pone.0189768.
  • Song Y, Garg S, Girotra M, Maddox C, von Rosenvinge EC, Dutta A, Dutta S, Fricke WF. Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent Clostridium difficile infection. PLoS One. 2013;8(11):e81330. doi:10.1371/journal.pone.0081330.
  • Zuo T, Wong SH, Cheung CP, Lam K, Lui R, Cheung K, Zhang F, Tang W, Ching JYL, Wu JCY, et al. Gut fungal dysbiosis correlates with reduced efficacy of fecal microbiota transplantation in Clostridium difficile infection. Nat Commun. 2018;9(1):3663. doi:10.1038/s41467-018-06103-6.
  • Staley C, Vaughn BP, Graiziger CT, Sadowsky MJ, Khoruts A. Gut-sparing treatment of urinary tract infection in patients at high risk of Clostridium difficile infection. J Antimicrob Chemother. 2017;72(2):522–528. doi:10.1093/jac/dkw499.
  • Staley C, Kaiser T, Vaughn BP, Graiziger CT, Hamilton MJ, Rehman TU, Song K, Khoruts A, Sadowsky MJ. Predicting recurrence of Clostridium difficile infection following encapsulated fecal microbiota transplantation. Microbiome. 2018;6(1):166. doi:10.1186/s40168-018-0549-6.
  • Holmes I, Harris K, Quince C, Gilbert JA. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One. 2012;7(2):e30126. doi:10.1371/journal.pone.0030126.
  • Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nat Rev Microbiol. 2016;14(1):20–32. doi:10.1038/nrmicro3552.
  • Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2(2):119–129. doi:10.1016/j.chom.2007.06.010.
  • Kirsner JB, Shorter RG. Recent developments in ”nonspecific” inflammatory bowel disease (first of two parts). N Engl J Med. 1982;306(13):775–785. doi:10.1056/NEJM198204013061304.
  • Shenhav L, Thompson M, Joseph TA, Briscoe L, Furman O, Bogumil D, Mizrahi I, Pe’er I, Halperin E. FEAST: fast expectation-maximization for microbial source tracking. Nat Methods. 2019;16(7):627–632. doi:10.1038/s41592-019-0431-x.
  • Kong L, Lloyd-Price J, Vatanen T, Seksik P, Beaugerie L, Simon T, Vlamakis H, Sokol H, Xavier RJ. Linking strain engraftment in fecal microbiota transplantation with maintenance of remission in Crohn’s disease. Gastroenterology. 2020;159(6):2193–2202 e5. doi:10.1053/j.gastro.2020.08.045.
  • Hernandez M, de Frutos M, Rodríguez-Lázaro D, López-Urrutia L, Quijada NM, Eiros JM. Fecal microbiota of toxigenic clostridioides difficile-associated diarrhea. Front Microbiol. 2018;9:3331. doi:10.3389/fmicb.2018.03331.
  • Costea PI, Hildebrand F, Arumugam M, Bäckhed F, Blaser MJ, Bushman FD, De vos WM, Ehrlich S, Fraser CM, Hattori M, et al. Enterotypes in the landscape of gut microbial community composition. Nat Microbiol. 2018;3(1):8–16. doi:10.1038/s41564-017-0072-8.
  • Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9.
  • Lee STM, Kahn SA, Delmont TO, Shaiber A, Esen ÖC, Hubert NA, Morrison HG, Antonopoulos DA, Rubin DT, Eren AM, et al. Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics. Microbiome. 2017;5(1):50. doi:10.1186/s40168-017-0270-x.
  • Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol. 2014;121:91–119.
  • Kellingray L, Gall GL, Defernez M, Beales ILP, Franslem-Elumogo N, Narbad A. Microbial taxonomic and metabolic alterations during faecal microbiota transplantation to treat Clostridium difficile infection. J Infect. 2018;77(2):107–118. doi:10.1016/j.jinf.2018.04.012.
  • Cammarota G, Ianiro G, Tilg H, Rajilić-Stojanović 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(4):569–580. doi:10.1136/gutjnl-2016-313017.
  • 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(1):102–109 e6. doi:10.1053/j.gastro.2015.04.001.
  • Earley H, Lennon G, Balfe Á, Coffey JC, Winter DC, O’Connell PR. The abundance of Akkermansia muciniphila and its relationship with sulphated colonic mucins in health and ulcerative colitis. Sci Rep. 2019;9(1):15683. doi:10.1038/s41598-019-51878-3.
  • 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(1):3. doi:10.1186/2049-2618-1-3.
  • Emanuelsson F, Claesson BEB, Ljungström L, Tvede M, Ung K-A. Faecal microbiota transplantation and bacteriotherapy for recurrent Clostridium difficile infection: a retrospective evaluation of 31 patients. Scand J Infect Dis. 2014;46(2):89–97. doi:10.3109/00365548.2013.858181.
  • Fang H, Fu L, Wang J. Protocol for fecal microbiota transplantation in inflammatory bowel disease: a systematic review and meta-analysis. Biomed Res Int. 2018;2018:8941340. doi:10.1155/2018/8941340.
  • Aggarwala V, Mogno I, Li Z, Yang C, Britton GJ, Chen-Liaw A, Mitcham J, Bongers G, Gevers D, Clemente JC, et al. Precise quantification of bacterial strains after fecal microbiota transplantation delineates long-term engraftment and explains outcomes. Nat Microbiol. 2021;6(10):1309–1318. doi:10.1038/s41564-021-00966-0.
  • Hjorth MF, Blædel T, Bendtsen LQ, Lorenzen JK, Holm JB, Kiilerich P, Roager HM, Kristiansen K, Larsen LH, Astrup A, et al. Prevotella-to-Bacteroides ratio predicts body weight and fat loss success on 24-week diets varying in macronutrient composition and dietary fiber: results from a post-hoc analysis. Int J Obes (Lond). 2019;43(1):149–157. doi:10.1038/s41366-018-0093-2.
  • Ding X, Li Q, Li P, Zhang T, Cui B, Ji G, Lu X, Zhang F. Long-term safety and efficacy of fecal microbiota transplant in active ulcerative colitis. Drug Saf. 2019;42(7):869–880. doi:10.1007/s40264-019-00809-2.
  • Fecal Microbiota Transplantation-standardization Study Group. Nanjing consensus on methodology of washed microbiota transplantation. Chin Med J (Engl). 2020;133(19):2330–2332. doi:10.1097/CM9.0000000000000954.
  • Zhang T, Lu G, Zhao Z, Liu Y, Shen Q, Li P, Chen Y, Yin H, Wang H, Marcella C, et al. Washed microbiota transplantation vs. manual fecal microbiota transplantation: clinical findings, animal studies and in vitro screening. Protein Cell. 2020;11(4):251–266. doi:10.1007/s13238-019-00684-8.
  • Yang J, Hou L, Wang J, Xiao L, Zhang J, Yin N, Yao S, Cheng K, Zhang W, Shi Z, et al. Unfavourable intrauterine environment contributes to abnormal gut microbiome and metabolome in twins. Gut. 2022;gutjnl-2021–326482. doi:10.1136/gutjnl-2021-326482
  • Wang J, Zheng J, Shi W, Du N, Xu X, Zhang Y, Ji P, Zhang F, Jia Z, Wang Y, et al. Dysbiosis of maternal and neonatal microbiota associated with gestational diabetes mellitus. Gut. 2018;67(9):1614–1625. doi:10.1136/gutjnl-2018-315988.
  • Wang J, Jia Z, Zhang B, Peng L, Zhao F. Tracing the accumulation of in vivo human oral microbiota elucidates microbial community dynamics at the gateway to the GI tract. Gut. 2020;69(7):1355–1356. doi:10.1136/gutjnl-2019-318977.
  • Xiao L, Zhang F, Zhao F. Large-scale microbiome data integration enables robust biomarker identification. Nature Comput Sci. 2022;2(5):307–316. doi:10.1038/s43588-022-00247-8.
  • Xiao L, Wang J, Zheng J, Li X, Zhao F. Deterministic transition of enterotypes shapes the infant gut microbiome at an early age. Genome Biol. 2021;22(1):243. doi:10.1186/s13059-021-02463-3.
  • Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957–2963. doi:10.1093/bioinformatics/btr507.
  • Chen S, Huang T, Zhou Y, Han Y, Xu M, Gu J. AfterQC: automatic filtering, trimming, error removing and quality control for fastq data. BMC Bioinform. 2017;18(Suppl 3):80. doi:10.1186/s12859-017-1469-3.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi:10.1038/nmeth.f.303.
  • Wirbel J, Pyl PT, Kartal E, Zych K, Kashani A, Milanese A, Fleck JS, Voigt AY, Palleja A, Ponnudurai R, et al. Meta-analysis of fecal metagenomes reveals global microbial signatures that are specific for colorectal cancer. Nat Med. 2019;25(4):679–689. doi:10.1038/s41591-019-0406-6.
  • Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto J-M, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi:10.1038/nature09944.