Advertisement

Current Hematologic Malignancy Reports

, Volume 11, Issue 1, pp 19–28 | Cite as

Microbiota Manipulation With Prebiotics and Probiotics in Patients Undergoing Stem Cell Transplantation

  • Tessa M. Andermann
  • Andrew Rezvani
  • Ami S. Bhatt
Stem Cell Transplantation (R Maziarz, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Stem Cell Transplantation

Abstract

Hematopoietic stem cell transplantation (HSCT) is a potentially life-saving therapy that often comes at the cost of complications such as graft-versus-host disease and post-transplant infections. With improved technology to understand the ecosystem of microorganisms (viruses, bacteria, fungi, and microeukaryotes) that make up the gut microbiota, there is increasing evidence of the microbiota’s contribution to the development of post-transplant complications. Antibiotics have traditionally been the mainstay of microbiota-altering therapies available to physicians. Recently, interest is increasing in the use of prebiotics and probiotics to support the development and sustainability of a healthier microbiota. In this review, we will describe the evidence for the use of prebiotics and probiotics in combating microbiota dysbiosis and explore the ways in which they may be used in future research to potentially improve clinical outcomes and decrease rates of graft-versus-host disease (GVHD) and post-transplant infection.

Keywords

Hematopoietic stem cell transplantation Graft-versus-host disease Post-transplant infection 

Notes

Acknowledgments

This work was made possible by the following awards: American Society of Hematology Scholar Award (A.S.B.), Amy Strelzer Manasevit award (National Marrow Donor Program and Be The Match foundation) (A.S.B.), NCI K08 CA184420 (A.S.B), the American Cancer Society Mentored Research Scholar Grant 122663-MRSG-12-162-01-LIB (A. R.), and NIH T32 AI007502 (T.M.A.). The authors would also like to thank Dr. Lucy Tompkins from the Division of Infectious Diseases at Stanford University for her review of the manuscript and figures.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449:804–10.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–9.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Morgan XC, Huttenhower C. Meta’omic analytic techniques for studying the intestinal microbiome. Gastroenterology. 2014;146:1437–48.e1.CrossRefPubMedGoogle Scholar
  5. 5.•
    Bhatt AS, Freeman SS, Herrera AF, Pedamallu CS, Gevers D, Duke F, et al. Sequence-based discovery of Bradyrhizobium enterica in cord colitis syndrome. N Engl J Med. 2013;369:517–28. Bhatt et al. used next-generation shotgun sequencing in the characterization of the microbiome in umbilical cord HSCT transplant patients with cord colitis and identified a novel pathogen, Bradyrhizobium enterica , responsible for disease in these patients.Google Scholar
  6. 6.
    Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010;107:12204–9.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9:313–23.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Kamada N, Kim Y-G, Sham HP, Vallance BA, Puente JL, Martens EC, et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 2012;336:1325–9.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620–5.CrossRefPubMedGoogle Scholar
  10. 10.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRefPubMedGoogle Scholar
  11. 11.
    Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014;514:181–6.PubMedGoogle Scholar
  12. 12.
    Collins SM. A role for the gut microbiota in IBS. Nat Rev Gastroenterol Hepatol. 2014;11:497–505.CrossRefPubMedGoogle Scholar
  13. 13.
    Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155:1451–63.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Taur Y, Pamer EG. The intestinal microbiota and susceptibility to infection in immunocompromised patients. Curr Opin Infect Dis. 2013;26:332–7.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.••
    Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J, Gobourne A, et al. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis Off Publ Infect Dis Soc Am. 2012;55:905–14. Taur et al. showed the reduction of intestinal microbiota diversity following allogeneic HSCT. Those patients with reduced microbiota diversity often developed microbiota domination by a single bacterial taxon leading to an increased risk of bacteremia with the dominant organism.CrossRefGoogle Scholar
  16. 16.••
    Taur Y, Jenq RR, Perales M-A, Littmann ER, Morjaria S, Ling L, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. 2014;124:1174–82. Taur et al. demonstrated that intestinal microbiota diversity was an independent predictor of mortality in patients undergoing allogeneic HSCT. Patients with low microbiota diversity were found to have higher all-cause mortality.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.••
    Holler E, Butzhammer P, Schmid K, Hundsrucker C, Koestler J, Peter K, et al. Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2014;20:640–5. Holler et al. found an association between the loss of diversity in the intestinal microbiota following the use of antibiotics during allogeneic HSCT and the development of acute gastrointestinal GVHD.CrossRefGoogle Scholar
  18. 18.
    Gooley TA, Chien JW, Pergam SA, Hingorani S, Sorror ML, Boeckh M, et al. Reduced mortality after allogeneic hematopoietic-cell transplantation. N Engl J Med. 2010;363:2091–101.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Arai S, Arora M, Wang T, Spellman SR, He W, Couriel DR, et al. Increasing incidence of chronic graft-versus-host disease in allogeneic transplantation: a report from the Center for International Blood and Marrow Transplant Research. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2015;21:266–74.CrossRefGoogle Scholar
  20. 20.
    Wolff D, Gerbitz A, Ayuk F, Kiani A, Hildebrandt GC, Vogelsang GB, et al. Consensus conference on clinical practice in chronic graft-versus-host disease (GVHD): first-line and topical treatment of chronic GVHD. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2010;16:1611–28.CrossRefGoogle Scholar
  21. 21.
    Jones JM, Wilson R, Bealmear PM. Mortality and gross pathology of secondary disease in germfree mouse radiation chimeras. Radiat Res. 1971;45:577–88.CrossRefPubMedGoogle Scholar
  22. 22.
    van Bekkum DW, Roodenburg J, Heidt PJ, van der Waaij D. Mitigation of secondary disease of allogeneic mouse radiation chimeras by modification of the intestinal microflora. J Natl Cancer Inst. 1974;52:401–4.PubMedGoogle Scholar
  23. 23.
    Navari RM, Buckner CD, Clift RA, Storb R, Sanders JE, Stewart P, et al. Prophylaxis of infection in patients with aplastic anemia receiving allogeneic marrow transplants. Am J Med. 1984;76:564–72.CrossRefPubMedGoogle Scholar
  24. 24.
    Vossen JM, Guiot HFL, Lankester AC, Vossen ACTM, Bredius RGM, Wolterbeek R, et al. Complete suppression of the gut microbiome prevents acute graft-versus-host disease following allogeneic bone marrow transplantation. PLoS One. 2014;9:e105706.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Beelen DW, Elmaagacli A, Müller K-D, Hirche H, Schaefer UW. Influence of intestinal bacterial decontamination using metronidazole and ciprofloxacin or ciprofloxacin alone on the development of acute graft-versus-host disease after marrow transplantation in patients with hematologic malignancies: final results and long-term follow-up of an open-label prospective randomized trial. Blood. 1999;93:3267–75.PubMedGoogle Scholar
  26. 26.
    Russell JA, Chaudhry A, Booth K, Brown C, Woodman RC, Valentine K, et al. Early outcomes after allogeneic stem cell transplantation for leukemia and myelodysplasia without protective isolation: a 10-year experience. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2000;6:109–14.CrossRefGoogle Scholar
  27. 27.••
    Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, et al. Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2015;21:1373–83. Jenq et al. demonstrated that increased microbiota diversity during transplant was associated with the decreased acute GVHD and lower GVHD-related mortality. This resistance to GVHD and GVHD-related mortality was mediated by the abundance of Blautia within the intestinal microbiota.CrossRefGoogle Scholar
  28. 28.
    Manzo VE, Bhatt AS. The human microbiome in hematopoiesis and hematologic disorders. Blood. 2015;126:311–8.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Mathewson N, Reddy P. The microbiome and graft versus host disease. Curr Stem Cell Rep. 2015;1:39–47.CrossRefGoogle Scholar
  30. 30.
    Shono Y, Docampo MD, Peled JU, Perobelli SM, Jenq RR. Intestinal microbiota-related effects on graft-versus-host disease. Int J Hematol. 2015;101:428–37.CrossRefPubMedGoogle Scholar
  31. 31.
    Docampo MD, Auletta JJ, Jenq RR. Emerging influence of the intestinal microbiota during allogeneic hematopoietic cell transplantation: control the Gut and the body will follow. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2015;21:1360–6.CrossRefGoogle Scholar
  32. 32.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Roberfroid MB. Introducing inulin-type fructans. Br J Nutr. 2005;93 Suppl 1:S13–25.CrossRefPubMedGoogle Scholar
  34. 34.
    Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73.CrossRefPubMedGoogle Scholar
  35. 35.
    Peng L, He Z, Chen W, Holzman IR, Lin J. Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr Res. 2007;61:37–41.CrossRefPubMedGoogle Scholar
  36. 36.
    Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity. 2014;40:833–42.CrossRefPubMedGoogle Scholar
  37. 37.
    Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282–6.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lecerf J-M, Dépeint F, Clerc E, Dugenet Y, Niamba CN, Rhazi L, et al. Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties. Br J Nutr. 2012;108:1847–58.CrossRefPubMedGoogle Scholar
  39. 39.
    Childs CE, Röytiö H, Alhoniemi E, Fekete AA, Forssten SD, Hudjec N, et al. Xylo-oligosaccharides alone or in synbiotic combination with Bifidobacterium animalis subsp. lactis induce bifidogenesis and modulate markers of immune function in healthy adults: a double-blind, placebo-controlled, randomised, factorial cross-over study. Br. J. Nutr. 2014: 1–12.Google Scholar
  40. 40.
    Bouhnik Y, Raskine L, Simoneau G, Vicaut E, Neut C, Flourié B, et al. The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose–response relation study. Am J Clin Nutr. 2004;80:1658–64.PubMedGoogle Scholar
  41. 41.
    Vulevic J, Juric A, Walton GE, Claus SP, Tzortzis G, Toward RE, et al. Influence of galacto-oligosaccharide mixture (B-GOS) on gut microbiota, immune parameters and metabonomics in elderly persons. Br. J. Nutr. 2015: 1–10.Google Scholar
  42. 42.
    Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 2007;104:13780–5.Google Scholar
  43. 43.
    Hafer A, Krämer S, Duncker S, Krüger M, Manns MP, Bischoff SC. Effect of oral lactulose on clinical and immunohistochemical parameters in patients with inflammatory bowel disease: a pilot study. BMC Gastroenterol. 2007;7:36.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Joossens M, De Preter V, Ballet V, Verbeke K, Rutgeerts P, Vermeire S. Effect of oligofructose-enriched inulin (OF-IN) on bacterial composition and disease activity of patients with Crohn’s disease: results from a double-blinded randomised controlled trial. Gut. 2012;61:958.CrossRefPubMedGoogle Scholar
  45. 45.
    Benjamin JL, Hedin CRH, Koutsoumpas A, Ng SC, McCarthy NE, Hart AL, et al. Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn’s disease. Gut. 2011;60:923–9.CrossRefPubMedGoogle Scholar
  46. 46.
    Casellas F, Borruel N, Torrejón A, Varela E, Antolin M, Guarner F, et al. Oral oligofructose-enriched inulin supplementation in acute ulcerative colitis is well tolerated and associated with lowered faecal calprotectin. Aliment Pharmacol Ther. 2007;25:1061–7.CrossRefPubMedGoogle Scholar
  47. 47.
    Lindsay JO, Whelan K, Stagg AJ, Gobin P, Al-Hassi HO, Rayment N, et al. Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn’s disease. Gut. 2006;55:348–55.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK. Host-bacterial symbiosis in health and disease. Adv Immunol. 2010;107:243–74.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Iyama S, Sato T, Tatsumi H, Hashimoto A, Tatekoshi A, Kamihara Y, et al. Efficacy of enteral supplementation enriched with glutamine, fiber, and oligosaccharide on mucosal injury following hematopoietic stem cell transplantation. Case Rep Oncol. 2014;7:692–9.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Szeluga DJ, Stuart RK, Brookmeyer R, Utermohlen V, Santos GW. Nutritional support of bone marrow transplant recipients: a prospective, randomized clinical trial comparing total parenteral nutrition to an enteral feeding program. Cancer Res. 1987;47:3309–16.PubMedGoogle Scholar
  51. 51.
    van der Meij BS, de Graaf P, Wierdsma NJ, Langius JAE, Janssen JJWM, van Leeuwen PAM, et al. Nutritional support in patients with GVHD of the digestive tract: state of the art. Bone Marrow Transplant. 2013;48:474–82.CrossRefPubMedGoogle Scholar
  52. 52.
    Lye AD, Hayslip JW. Immunonutrition: does it have a role in improving recovery in patients receiving a stem cell transplant? Nutr Cancer. 2012;64:503–7.CrossRefPubMedGoogle Scholar
  53. 53.
    Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146:1564–72.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Goldenberg JZ, Ma SSY, Saxton JD, Martzen MR, Vandvik PO, Thorlund K, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Syst Rev. 2013;5:CD006095.PubMedGoogle Scholar
  55. 55.
    Cremonini F, Di Caro S, Covino M, Armuzzi A, Gabrielli M, Santarelli L, et al. Effect of different probiotic preparations on anti-helicobacter pylori therapy-related side effects: a parallel group, triple blind, placebo-controlled study. Am J Gastroenterol. 2002;97:2744–9.CrossRefPubMedGoogle Scholar
  56. 56.
    Beniwal RS, Arena VC, Thomas L, Narla S, Imperiale TF, Chaudhry RA, et al. A randomized trial of yogurt for prevention of antibiotic-associated diarrhea. Dig Dis Sci. 2003;48:2077–82.CrossRefPubMedGoogle Scholar
  57. 57.
    Kotowska M, Albrecht P, Szajewska H. Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in children: a randomized double-blind placebo-controlled trial. Aliment Pharmacol Ther. 2005;21:583–90.CrossRefPubMedGoogle Scholar
  58. 58.
    Guandalini S, Pensabene L, Zikri MA, Dias JA, Casali LG, Hoekstra H, et al. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr. 2000;30:54–60.CrossRefPubMedGoogle Scholar
  59. 59.
    Margreiter M, Ludl K, Phleps W, Kaehler ST. Therapeutic value of a Lactobacillus gasseri and Bifidobacterium longum fixed bacterium combination in acute diarrhea: a randomized, double-blind, controlled clinical trial. Int J Clin Pharmacol Ther. 2006;44:207–15.CrossRefPubMedGoogle Scholar
  60. 60.
    Niedzielin K, Kordecki H, Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol. 2001;13:1143–7.CrossRefPubMedGoogle Scholar
  61. 61.
    Kajander K, Hatakka K, Poussa T, Färkkilä M, Korpela R. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther. 2005;22:387–94.CrossRefPubMedGoogle Scholar
  62. 62.
    Enck P, Zimmermann K, Menke G, Müller-Lissner S, Martens U, Klosterhalfen S. A mixture of Escherichia coli (DSM 17252) and Enterococcus faecalis (DSM 16440) for treatment of the irritable bowel syndrome--a randomized controlled trial with primary care physicians. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2008;20:1103–9.CrossRefGoogle Scholar
  63. 63.
    Cui S, Hu Y. Multistrain probiotic preparation significantly reduces symptoms of irritable bowel syndrome in a double-blind placebo-controlled study. Int J Clin Exp Med. 2012;5:238–44.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Dapoigny M, Piche T, Ducrotte P, Lunaud B, Cardot J-M, Bernalier-Donadille A. Efficacy and safety profile of LCR35 complete freeze-dried culture in irritable bowel syndrome: a randomized, double-blind study. World J Gastroenterol WJG. 2012;18:2067–75.CrossRefPubMedGoogle Scholar
  65. 65.
    Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T. Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr. 2003;22:56–63.CrossRefPubMedGoogle Scholar
  66. 66.
    Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut. 2004;53:1617–23.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Lin H-C, Hsu C-H, Chen H-L, Chung M-Y, Hsu J-F, Lien R, et al. Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a multicenter, randomized, controlled trial. Pediatrics. 2008;122:693–700.CrossRefPubMedGoogle Scholar
  68. 68.
    Manzoni P, Mostert M, Leonessa ML, Priolo C, Farina D, Monetti C, et al. Oral supplementation with Lactobacillus casei subspecies rhamnosus prevents enteric colonization by Candida species in preterm neonates: a randomized study. Clin Infect Dis Off Publ Infect Dis Soc Am. 2006;42:1735–42.CrossRefGoogle Scholar
  69. 69.
    Fernández-Carrocera LA, Solis-Herrera A, Cabanillas-Ayón M, Gallardo-Sarmiento RB, García-Pérez CS, Montaño-Rodríguez R, et al. Double-blind, randomised clinical assay to evaluate the efficacy of probiotics in preterm newborns weighing less than 1500 g in the prevention of necrotising enterocolitis. Arch Dis Child Fetal Neonatal Ed. 2013;98:F5–9.CrossRefPubMedGoogle Scholar
  70. 70.
    Yang Y-X, He M, Hu G, Wei J, Pages P, Yang X-H, et al. Effect of a fermented milk containing Bifidobacterium lactis DN-173010 on Chinese constipated women. World J Gastroenterol WJG. 2008;14:6237–43.CrossRefPubMedGoogle Scholar
  71. 71.
    Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D, Bazzocchi G, et al. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology. 2000;119:305–9.CrossRefPubMedGoogle Scholar
  72. 72.
    Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers KM, Brigidi P, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology. 2003;124:1202–9.CrossRefPubMedGoogle Scholar
  73. 73.
    Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S, Talbot IC, et al. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut. 2004;53:108–14.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Van Gossum A, Dewit O, Louis E, de Hertogh G, Baert F, Fontaine F, et al. Multicenter randomized-controlled clinical trial of probiotics (Lactobacillus johnsonii, LA1) on early endoscopic recurrence of Crohn’s disease after lleo-caecal resection. Inflamm Bowel Dis. 2007;13:135–42.CrossRefPubMedGoogle Scholar
  75. 75.
    Vitetta L, Briskey D, Alford H, Hall S, Coulson S. Probiotics, prebiotics and the gastrointestinal tract in health and disease. Inflammopharmacology. 2014;22:135–54.CrossRefPubMedGoogle Scholar
  76. 76.
    Preidis GA, Versalovic J. Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology. 2009;136:2015–31.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Ghouri YA, Richards DM, Rahimi EF, Krill JT, Jelinek KA, DuPont AW. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol. 2014;7:473–87.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004;53:1602–9.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Drekonja D, Reich J, Gezahegn S, Greer N, Shaukat A, MacDonald R, et al. Fecal microbiota transplantation for clostridium difficile infection: a systematic review. Ann Intern Med. 2015;162:630–8.CrossRefPubMedGoogle Scholar
  80. 80.
    Ianiro G, Bibbò S, Scaldaferri F, Gasbarrini A, Cammarota G. Fecal microbiota transplantation in inflammatory bowel disease: beyond the excitement. Medicine (Baltimore). 2014;93:e97.CrossRefGoogle Scholar
  81. 81.
    Quera R, Espinoza R, Estay C, Rivera D. Bacteremia as an adverse event of fecal microbiota transplantation in a patient with Crohn’s disease and recurrent Clostridium difficile infection. J Crohns Colitis. 2014;8:252–3.CrossRefPubMedGoogle Scholar
  82. 82.
    Schwartz M, Gluck M, Koon S. Norovirus gastroenteritis after fecal microbiota transplantation for treatment of clostridium difficile infection despite asymptomatic donors and lack of sick contacts. Am J Gastroenterol. 2013;108:1367.CrossRefPubMedGoogle Scholar
  83. 83.
    Gerbitz A, Schultz M, Wilke A, Linde H-J, Schölmerich J, Andreesen R, et al. Probiotic effects on experimental graft-versus-host disease: let them eat yogurt. Blood. 2004;103:4365–7.CrossRefPubMedGoogle Scholar
  84. 84.
    Mittal C, Miller N, Meighani A, Hart BR, John A, Ramesh M. Fecal microbiota transplant for recurrent Clostridium difficile infection after peripheral autologous stem cell transplant for diffuse large B-cell lymphoma. Bone Marrow Transplant. 2015;50:1010.CrossRefPubMedGoogle Scholar
  85. 85.
    de Castro CG, Ganc AJ, Ganc RL, Petrolli MS, Hamerschlack N. Fecal microbiota transplant after hematopoietic SCT: report of a successful case. Bone Marrow Transplant. 2015;50:145.CrossRefPubMedGoogle Scholar
  86. 86.
    Neemann K, Eichele DD, Smith PW, Bociek R, Akhtari M, Freifeld A. Fecal microbiota transplantation for fulminant Clostridium difficile infection in an allogeneic stem cell transplant patient. Transpl Infect Dis Off J Transplant Soc. 2012;14:E161–5.CrossRefGoogle Scholar
  87. 87.
    Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet Lond Engl. 1989;1:1156–60.CrossRefGoogle Scholar
  88. 88.
    Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: “RePOOPulating” the gut. Microbiome. 2013;1:3.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Miquel S, Martín R, Rossi O, Bermúdez-Humarán LG, Chatel JM, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16:255–61.CrossRefPubMedGoogle Scholar
  91. 91.
    Khan MT, van Dijl JM, Harmsen HJM. Antioxidants keep the potentially probiotic but highly oxygen-sensitive human Gut bacterium faecalibacterium prausnitzii alive at ambient Air. PLoS ONE. 2014;9:e96097.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013;500:232–6.CrossRefPubMedGoogle Scholar
  93. 93.••
    Buffie CG, Bucci V, Stein RR, McKenney PT, Ling L, Gobourne A, et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature. 2015;517:205–8. Buffie et al. found that the intestinal organism Clostridium scindens conferred resistance to Clostridium difficile in patients undergoing allogeneic HSCT as well as in a murine model. They further demonstrated that Clostridium scindens resistance is dependent on the synthesis of secondary bile salts, demonstrating a potential avenue for the development of precision microbiota-based therapeutics.Google Scholar
  94. 94.
    Aas J, Gessert CE, Bakken JS. Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis Off Publ Infect Dis Soc Am. 2003;36:580–5.CrossRefGoogle Scholar
  95. 95.
    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;107:761–7.CrossRefPubMedGoogle Scholar
  96. 96.
    Zainah H, Silverman A. Fecal bacteriotherapy: a case report in an immunosuppressed patient with ulcerative colitis and recurrent clostridium difficile infection. Case Rep Infect Dis. 2012;2012:810943.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Duplessis CA, You D, Johnson M, Speziale A. Efficacious outcome employing fecal bacteriotherapy in severe Crohn’s colitis complicated by refractory Clostridium difficile infection. Infection. 2012;40:469–72.CrossRefPubMedGoogle Scholar
  98. 98.
    Pathak R, Enuh HA, Patel A, Wickremesinghe P. Treatment of relapsing Clostridium difficile infection using fecal microbiota transplantation. Clin Exp Gastroenterol. 2013;7:1–6.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Friedman-Moraco RJ, Mehta AK, Lyon GM, Kraft CS. Fecal microbiota transplantation for refractory Clostridium difficile colitis in solid organ transplant recipients. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2014;14:477–80.CrossRefGoogle Scholar
  100. 100.
    Trubiano JA, George A, Barnett J, Siwan M, Heriot A, Prince HM, et al. A different kind of “allogeneic transplant”: successful fecal microbiota transplant for recurrent and refractory Clostridium difficile infection in a patient with relapsed aggressive B-cell lymphoma. Leuk Lymphoma. 2015;56:512–4.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Tessa M. Andermann
    • 1
  • Andrew Rezvani
    • 2
  • Ami S. Bhatt
    • 2
    • 3
    • 4
  1. 1.Department of Medicine, Division of Infectious DiseasesStanford UniversityStanfordUSA
  2. 2.Department of Medicine, Division of Blood and Marrow TransplantationStanford UniversityStanfordUSA
  3. 3.Department of Medicine, Division of HematologyStanford UniversityStanfordUSA
  4. 4.Department of GeneticsStanford UniversityStanfordUSA

Personalised recommendations