Internal and Emergency Medicine

, Volume 9, Issue 4, pp 365–373 | Cite as

Gut microbiota modulation: probiotics, antibiotics or fecal microbiota transplantation?

  • Giovanni Cammarota
  • Gianluca Ianiro
  • Stefano Bibbò
  • Antonio Gasbarrini
IM - REVIEW

Abstract

Gut microbiota is known to have a relevant role in our health, and is also related to both gastrointestinal and extradigestive diseases. Therefore, restoring the alteration of gut microbiota represents an outstanding clinical target for the treatment of gut microbiota-related diseases. The modulation of gut microbiota is perhaps an ancestral, innate concept for human beings. At this time, the restoration of gut microbiota impairment is a well-established concept in mainstream medicine, and several therapeutic approaches have been developed in this regard. Antibiotics, prebiotics and probiotics are the best known and commercially available options to overcome gastrointestinal dysbiosis. Fecal microbiota transplantation is an old procedure that has recently become popular again. It has shown a clear effectiveness in the treatment of C. difficile infection, and now represents a cutting-edge option for the restoration of gut microbiota. Nevertheless, such weapons should be used with caution. Antibiotics can indeed harm and alter gut microbiota composition. Probiotics, instead, are not at all the same thing, and thinking in terms of different strains is probably the only way to improve clinical outcomes. Moreover, fecal microbiota transplantation has shown promising results, but stronger proofs are needed. Considerable efforts are needed to increase our knowledge in the field of gut microbiota, especially with regard to the future use in its modulation for therapeutic purposes.

Keywords

Gut microbiota Gut microbiota modulation Antibiotics Probiotics Fecal microbiota transplantation 

Notes

Conflict of interest

None.

References

  1. 1.
    Bäckhed F, Ley RE, Sonnenburg JL et al (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920PubMedCrossRefGoogle Scholar
  2. 2.
    Turnbaugh PJ, Ley RE, Hamady M et al (2007) The human microbiome project. Nature 449:804–810PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Zoetendal EG, Rajilic-Stojanovic M, de Vos WM (2008) High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57:1605–1615PubMedCrossRefGoogle Scholar
  4. 4.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Arumugam M, Raes J, Pelletier E et al (2011) Enterotypes of the human gut microbiome. Nature 473:174–180PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Wu GD, Chen J, Hoffmann C et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334:105–108PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ (2013) Diet rapidly and reproducibly alters the human gut microbiome. Nature. doi: 10.1038/nature12820 (Epub ahead of print PMID: 24336217)
  9. 9.
    Palmer C, Bik EM, DiGiulio DB et al (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Spor A, Koren O, Ley RE (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9:279–290PubMedCrossRefGoogle Scholar
  11. 11.
    Costello EK, Lauber CL, Hamady M et al (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904. doi:10.1152/physrev.00045.2009 PubMedCrossRefGoogle Scholar
  13. 13.
    Manichanh C, Borruel N, Casellas F et al (2012) The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9:599–608PubMedCrossRefGoogle Scholar
  14. 14.
    Simrén M, Barbara G, Flint HJ, Spiegel BM, Spiller RC, Vanner S, Verdu EF, Whorwell PJ, Zoetendal EG, Rome Foundation Committee (2013) Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut 159–176. doi:10.1136/gutjnl-2012-302167 (Epub 2012 Jun 22. PMID: 22730468)
  15. 15.
    DuPont AW, DuPont HL (2011) The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastroenterol Hepatol 8(9):523–531. doi:10.1038/nrgastro.2011.133 (Review. PMID: 21844910)PubMedCrossRefGoogle Scholar
  16. 16.
    Zhu Q, Gao R, Wu W, Qin H (2013) The role of gut microbiota in the pathogenesis of colorectal cancer. Tumour Biol 34(3):1285–1300. doi:10.1007/s13277-013-0684-4 (Epub 2013 Feb 10. Review. PMID: 23397545)PubMedCrossRefGoogle Scholar
  17. 17.
    Aron-Wisnewsky J, Gaborit B, Dutour A, Clement K (2013) Gut microbiota and non-alcoholic fatty liver disease: new insights. Clin Microbiol Infect 19(4):338–348. doi:10.1111/1469-0691.12140 (Epub 2013 Mar 2. Review. PMID: 23452163)PubMedCrossRefGoogle Scholar
  18. 18.
    Dhiman RK (2013) Gut microbiota and hepatic encephalopathy. Metab Brain Dis 28(2):321–326. doi:10.1007/s11011-013-9388-0 (Epub 2013 Mar 6. Review. PMID: 23463489)PubMedCrossRefGoogle Scholar
  19. 19.
    Kovatcheva-Datchary P, Arora T (2013) Nutrition, the gut microbiome and the metabolic syndrome. Best Pract Res Clin Gastroenterol 27(1):59–72. doi:10.1016/j.bpg.2013.03.017 Review. PMID: 23768553PubMedCrossRefGoogle Scholar
  20. 20.
    Everard A, Cani PD (2013) Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol 27(1):73–83. doi:10.1016/j.bpg.2013.03.007 Review.PMID: 23768554PubMedCrossRefGoogle Scholar
  21. 21.
    Iebba V, Aloi M, Civitelli F, Cucchiara S (2011) Gut microbiota and pediatric disease. Dig Dis 29(6):531–539. doi:10.1159/000332969 (Epub 2011 Dec 12)PubMedCrossRefGoogle Scholar
  22. 22.
    Russell SL, Finlay BB (2012) The impact of gut microbes in allergic diseases. Curr Opin Gastroenterol 28(6):563–569. doi:10.1097/MOG.0b013e3283573017 (Review. PMID: 23010680)PubMedCrossRefGoogle Scholar
  23. 23.
    Leach J (2013) Gut microbiota: please pass the microbes. Nature 504(7478):33. doi:10.1038/504033c PubMedCrossRefGoogle Scholar
  24. 24.
    Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134:577–594PubMedCrossRefGoogle Scholar
  25. 25.
    Carroll IM, Ringel-Kulka T, Siddle JP, Ringel Y (2012) Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil 24(6):521–530, e248. doi: 10.1111/j.1365-2982.2012.01891.x (Epub 2012 Feb 20)
  26. 26.
    Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto JM, Kennedy S, Leonard P, Li J, Burgdorf K, Grarup N, Jørgensen T, Brandslund I, Nielsen HB, Juncker AS, Bertalan M, Levenez F, Pons N, Rasmussen S, Sunagawa S, Tap J, Tims S, Zoetendal EG, Brunak S, Clément K, Doré J, Kleerebezem M, Kristiansen K, Renault P, Sicheritz-Ponten T, de Vos WM, Zucker JD, Raes J, Hansen T, MetaHIT consortium, Bork P, Wang J, Ehrlich SD, Pedersen O (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500(7464):541–546. doi:10.1038/nature12506 PubMedCrossRefGoogle Scholar
  27. 27.
    Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009) A core gut microbiome in obese and lean twins. Nature 457(7228):480–484. doi:10.1038/nature07540 PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC (2013) Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. doi:10.1111/cea.12253 (Epub ahead of print PMID: 24330256)
  29. 29.
    Walker AW, Lawley TD (2013) Therapeutic modulation of intestinal dysbiosis. Pharmacol Res 69(1):75–86. doi:10.1016/j.phrs.2012.09.008 (Epub 2012 Sep 24. Review. PMID: 23017673)PubMedCrossRefGoogle Scholar
  30. 30.
    Cooper MA, Shlaes D (2011) Fix the antibiotics pipeline. Nature 472:32PubMedCrossRefGoogle Scholar
  31. 31.
    Megraud F, Coenen S, Versporten A, Kist M, Lopez-Brea M, Hirschl AM, Andersen LP, Goossens H, Glupczynski Y, Study Group participants (2013) Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut 62(1):34–42. doi:10.1136/gutjnl-2012-302254 (Epub 2012 May 12. PMID: 22580412)PubMedCrossRefGoogle Scholar
  32. 32.
    Jernberg C, Löfmark S, Edlund C, Jansson JK (2010) Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 156:3216–3223PubMedCrossRefGoogle Scholar
  33. 33.
    Hopkins MJ, Macfarlane GT (2003) Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro. Appl Environ Microbiol 69:1920–1927PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Stiemsma LT, Turvey SE, Finlay BB (2013) An antibiotic-altered microbiota provides fuel for the enteric foe. Cell Res. doi:10.1038/cr.2013.142 (Epub ahead of print)
  35. 35.
    Dollive S, Chen YY, Grunberg S, Bittinger K, Hoffmann C, Vandivier L, Cuff C, Lewis JD, Wu GD, Bushman FD (2013) Fungi of the murine gut: episodic variation and proliferation during antibiotic treatment. Plos One 8(8):e71806. doi:10.1371/journal.pone.0071806 PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Murphy R1, Stewart AW2, Braithwaite I3, Beasley R3, Hancox RJ4, Mitchell EA5; the ISAAC Phase Three Study Group (2013) Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes (Lond). doi:10.1038/ijo.2013.218 (Epub ahead of print)
  37. 37.
    Willing BP, Russell SL, Finlay BB (2011) Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol 9:233–243PubMedCrossRefGoogle Scholar
  38. 38.
    Modi SR, Lee HH, Spina CS, Collins JJ (2013) Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499(7457):219–222. doi:10.1038/nature12212 (Epub 2013 Jun 9)PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Schlundt J (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO/WHOGoogle Scholar
  40. 40.
    Dinleyici EC, Eren M, Ozen M, Yargic ZA, Vandenplas Y (2012) Effectiveness and safety of Saccharomyces boulardii for acute infectious diarrhea. Expert Opin Biol Ther 12(4):395–410. doi:10.1517/14712598.2012.664129 (Epub 2012 Feb 16. Review. PMID: 22335323)PubMedCrossRefGoogle Scholar
  41. 41.
    Ng SC et al (2009) Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15(2):300–310PubMedCrossRefGoogle Scholar
  42. 42.
    Hickson M (2013) Examining the evidence for the use of probiotics in clinical practice. Nurs Stand 27(29):35–41PubMedCrossRefGoogle Scholar
  43. 43.
    Bron PA, van Baarlen P, Kleerebezem M (2012) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10:66–78Google Scholar
  44. 44.
    Van Baarlen P, Troost F, van der Meer C et al (2011) Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc Natl Acad Sci USA 108(Suppl 1):4562–4569PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    O’Mahony L, McCarthy J, Kelly P et al (2005) Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128:541–551PubMedCrossRefGoogle Scholar
  46. 46.
    Shanahan F, Dinan TG, Ross P, Hill C (2012) Probiotics in transition. Clin Gastroenterol Hepatol 10(11):1220–1224. doi:10.1016/j.cgh.2012.09.020 (Epub 2012 Sep 23. Review. PMID: 23010563)PubMedCrossRefGoogle Scholar
  47. 47.
    Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412PubMedGoogle Scholar
  48. 48.
    Slavin J (2013) Fiber and prebiotics: mechanisms and health benefits. Nutrients 5(4):1417–1435. doi:10.3390/nu5041417 Review. PMID: 23609775PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Roberfroid MB (2007) Prebiotics: the concept revisited. J Nutr 137(3 Suppl 2):830S–837S (PMID 17311983)PubMedGoogle Scholar
  50. 50.
    Langlands SJ, Hopkins MJ, Coleman N, Cummings JH (2004) Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 53:1610–1616PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Duncan SH, Scott KP, Ramsay AG, Harmsen HJ, Welling GW, Stewart CS et al (2003) Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl Environ Microbiol 69:1136–1142PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    de Vrese M, Marteau PR (2007) Probiotics and prebiotics: effects on diarrhea. J Nutr 137(Suppl. 2):11S–803SGoogle Scholar
  53. 53.
    Zhang F, Luo W, Shi Y et al (2012) Should we standardize the 1700-year old fecal microbiota transplantation? Am J Gastroenterol 107:1755PubMedCrossRefGoogle Scholar
  54. 54.
    Borody TJ, Warren EF, Leis SM et al (2004) Bacteriotherapy using fecal flora: toying with human motions. J Clin Gastroenterol 38:475–483PubMedCrossRefGoogle Scholar
  55. 55.
    Lewis A (1999) Merde: excursions in scientific, cultural, and socio-historical coprology. Random House, New York, NYGoogle Scholar
  56. 56.
    Eiseman B, Silen W, Bascom GS et al (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44:854–859PubMedGoogle Scholar
  57. 57.
    Kelly CP, LaMont JT (2008) Clostridium difficile—more difficult than ever. N Engl J Med 359(18):1932–1940. doi:10.1056/NEJMra0707500 Review. PMID: 18971494PubMedCrossRefGoogle Scholar
  58. 58.
    Pepin J, Alary ME, Valiquette L et al (2005) Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clin Infect Dis 40:1591–1597PubMedCrossRefGoogle Scholar
  59. 59.
    Mattila E, Uusitalo-Seppälä R, Wuorela M, Lehtola L, Nurmi H, Ristikankare M, Moilanen V, Salminen K, Seppälä M, Mattila PS, Anttila VJ, Arkkila P (2012) Fecal transplantation, through colonoscopy, is effective therapy for recurrent Clostridium difficile infection. Gastroenterology 142(3):490–496. doi:10.1053/j.gastro.2011.11.037 (Epub 2011 Dec 7. PMID: 2215536)PubMedCrossRefGoogle Scholar
  60. 60.
    van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, Speelman P, Dijkgraaf MG, Keller JJ (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368(5):407–415. doi:10.1056/NEJMoa1205037 (Epub 2013 Jan 16. PMID: 23323867)PubMedCrossRefGoogle Scholar
  61. 61.
    O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7(7):688–693. doi:10.1038/sj.embor.7400731 PMC1500832PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(4):913–916.e7. doi:10.1053/j.gastro.2012.06.031 (PMID: 22728514)Google Scholar
  63. 63.
    Anderson JL, Edney RJ, Whelan K (2012) Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 36(6):503–516. doi:10.1111/j.1365-2036.2012.05220.x (Epub 2012 Jul 25. Review. PMID: 22827693)PubMedCrossRefGoogle Scholar
  64. 64.
    Grehan MJ, Borody TJ, Leis SM et al (2010) Durable alteration of the colonic microbiota by the administration of donor fecal flora. J Clin Gastroenterol 44:551–561PubMedCrossRefGoogle Scholar
  65. 65.
    Tannock G, Munro K, Harmsen H et al (2000) Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol 66:2578–2588PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Borody TJ, Khoruts A (2012) Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9:88–96CrossRefGoogle Scholar
  67. 67.
    Bakken JS, Borody T, Brandt LJ et al (2011) Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 9:1044–1049PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Cammarota G, Ianiro G, Gasbarrini A (2014) Fecal microbiota transplantation for the treatment of Clostridium difficile infection: a systematic review. J Clin Gastroenterol (Epub ahead of print)Google Scholar
  69. 69.
    Persky S, Brandt LJ (2000) Treatment of recurrent Clostridium difficile-associated diarrhea by administration of donated stool directly though a colonoscope. Am J Gastroenterol 95:3283–3285PubMedGoogle Scholar
  70. 70.
    Brandt LJ, Reddy SS (2011) Fecal microbiota transplantation for recurrent Clostridium difficile infection. J Clin Gastroenterol 45:S159–S167PubMedCrossRefGoogle Scholar
  71. 71.
    Silverman MS, Davis I, Pillai DR (2010) Success of self-administered home fecal transplantation for chronic Clostridium difficile infection. Clin Gastroenterol Hepatol 8:471–473PubMedCrossRefGoogle Scholar
  72. 72.
    Burns DA, Heap JT, Minton NP (2010) Clostridium difficile spore germination: an update. Res Microbiol 161:730–734PubMedCrossRefGoogle Scholar
  73. 73.
    Damman CJ, Miller SI, Surawicz CM, Zisman TL (2012) The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol 107(10):1452–1459. doi:10.1038/ajg.2012.93 PubMedCrossRefGoogle Scholar
  74. 74.
    Angelberger S, Reinisch W, Makristathis A, Lichtenberger C, Dejaco C, Papay P, Novacek G, Trauner M, Loy A, Berry D (2013) Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol 108(10):1620–1630. doi:10.1038/ajg.2013.257 (Epub 2013 Sep 24. PMID: 24060759)PubMedCrossRefGoogle Scholar
  75. 75.
    El-Matary W, Simpson R, Ricketts-Burns N (2012) Fecal microbiota transplantation: are we opening a can of worms? Gastroenterology 143:e19–e20PubMedCrossRefGoogle Scholar
  76. 76.
    Gough E, Shaikh H, Manges AR (2011) Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis 53:994–1002PubMedCrossRefGoogle Scholar
  77. 77.
    Brandt LJ (2013) Intestinal microbiota and the role of fecal microbiota transplant (FMT) in treatment of C. difficile infection. Am J Gastroenterol 108(2):177–185. doi:10.1038/ajg.2012.450 (Epub 2013 Jan 15. Review. PMID: 23318479)PubMedCrossRefGoogle Scholar
  78. 78.
    Smits LP, Bouter KE, de Vos WM, Borody TJ, Nieuwdorp M (2013) Therapeutic potential of fecal microbiota transplantation. Gastroenterology 145(5):946–953. doi:10.1053/j.gastro.2013.08.058 (Epub 2013 Sep 7. Review. PMID: 24018052)PubMedCrossRefGoogle Scholar
  79. 79.
    Aroniadis OC, Brandt LJ (2013) Fecal microbiota transplantation: past, present and future. Curr Opin Gastroenterol 29(1):79–84. doi:10.1097/MOG.0b013e32835a4b3e Review. PMID: 23041678PubMedCrossRefGoogle Scholar
  80. 80.
    Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A (2012) Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol 107:761–767PubMedCrossRefGoogle Scholar
  81. 81.
    Metchnikoff E, Mitchell PCS (1907) The prolongation of life: optimistic studies. William Heinemann, LondonGoogle Scholar

Copyright information

© SIMI 2014

Authors and Affiliations

  • Giovanni Cammarota
    • 1
    • 2
    • 3
  • Gianluca Ianiro
    • 1
    • 2
  • Stefano Bibbò
    • 1
    • 2
  • Antonio Gasbarrini
    • 1
    • 2
  1. 1.School of Medicine and SurgeryCatholic UniversityRomeItaly
  2. 2.Division of Internal Medicine and Gastroenterology, Department of Medical SciencesA. Gemelli University HospitalRomeItaly
  3. 3.A. Gemelli University HospitalRomeItaly

Personalised recommendations