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

Internal and Emergency Medicine

Volumn 9, Issue 4, 2014, Pages 365-373

  Cammarota, Giovanni ^a,b   Ianiro, Gianluca ^a,b   Bibbò, Stefano ^a,b   Gasbarrini, Antonio ^a,b  

^a CATHOLIC UNIVERSITY   (Italy)

^b FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

Author keywords

Antibiotics; Fecal microbiota transplantation; Gut microbiota; Gut microbiota modulation; Probiotics

Indexed keywords

ANTIINFECTIVE AGENT; PROBIOTIC AGENT;

DRUG EFFECTS; FECES; HUMAN; INTESTINE; MICROBIOLOGY; MICROFLORA;

ANTI-BACTERIAL AGENTS; FECES; HUMANS; INTESTINES; MICROBIOTA; PROBIOTICS;

EID: 84901508943     PISSN: 18280447     EISSN: 19709366     Source Type: Journal    
DOI: 10.1007/s11739-014-1069-4     Document Type: Review

References (81)

1. Bäckhed F, Ley RE, Sonnenburg JL et al (2005) Host-bacterial mutualism in the human intestine. Science 307: 1915-1920.
2. Turnbaugh PJ, Ley RE, Hamady M et al (2007) The human microbiome project. Nature 449: 804-810.
3. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM (2008) High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57: 1605-1615.
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): 59-65.
5. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415): 220-230.
6. Arumugam M, Raes J, Pelletier E et al (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180.
7. Wu GD, Chen J, Hoffmann C et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
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. Palmer C, Bik EM, DiGiulio DB et al (2007) Development of the human infant intestinal microbiota. PLoS Biol 5: e177.
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: 279-290.
11. Costello EK, Lauber CL, Hamady M et al (2009) Bacterial community variation in human body habitats across space and time. Science 326: 1694-1697.
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.
13. Manichanh C, Borruel N, Casellas F et al (2012) The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9: 599-608.
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. 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).
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).
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).
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).
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: 23768553.
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: 23768554.
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).
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).
23. Leach J (2013) Gut microbiota: please pass the microbes. Nature 504(7478): 33. doi: 10. 1038/504033c.
24. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
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. 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.
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.
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. 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).
30. Cooper MA, Shlaes D (2011) Fix the antibiotics pipeline. Nature 472: 32.
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).
32. Jernberg C, Löfmark S, Edlund C, Jansson JK (2010) Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology 156: 3216-3223.
33. Hopkins MJ, Macfarlane GT (2003) Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro. Appl Environ Microbiol 69: 1920-1927.
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. 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.
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. Willing BP, Russell SL, Finlay BB (2011) Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat Rev Microbiol 9: 233-243.
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).
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/WHO.
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).
41. Ng SC et al (2009) Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15(2): 300-310.
42. Hickson M (2013) Examining the evidence for the use of probiotics in clinical practice. Nurs Stand 27(29): 35-41.
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: 66-78.
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): 4562-4569.
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: 541-551.
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).
47. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125: 1401-1412.
48. Slavin J (2013) Fiber and prebiotics: mechanisms and health benefits. Nutrients 5(4): 1417-1435. doi: 10. 3390/nu5041417 Review. PMID: 23609775.
49. Roberfroid MB (2007) Prebiotics: the concept revisited. J Nutr 137(3 Suppl 2): 830S-837S (PMID 17311983).
50. Langlands SJ, Hopkins MJ, Coleman N, Cummings JH (2004) Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 53: 1610-1616.
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: 1136-1142.
52. de Vrese M, Marteau PR (2007) Probiotics and prebiotics: effects on diarrhea. J Nutr 137(Suppl. 2): 11S-803S.
53. Zhang F, Luo W, Shi Y et al (2012) Should we standardize the 1700-year old fecal microbiota transplantation? Am J Gastroenterol 107: 1755.
54. Borody TJ, Warren EF, Leis SM et al (2004) Bacteriotherapy using fecal flora: toying with human motions. J Clin Gastroenterol 38: 475-483.
55. Lewis A (1999) Merde: excursions in scientific, cultural, and socio-historical coprology. Random House, New York, NY.
56. Eiseman B, Silen W, Bascom GS et al (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44: 854-859.
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: 18971494.
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: 1591-1597.
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).
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).
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 PMC1500832.
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).
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).
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: 551-561.
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: 2578-2588.
66. Borody TJ, Khoruts A (2012) Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 9: 88-96.
67. Bakken JS, Borody T, Brandt LJ et al (2011) Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 9: 1044-1049.
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).
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: 3283-3285.
70. Brandt LJ, Reddy SS (2011) Fecal microbiota transplantation for recurrent Clostridium difficile infection. J Clin Gastroenterol 45: S159-S167.
71. Silverman MS, Davis I, Pillai DR (2010) Success of self-administered home fecal transplantation for chronic Clostridium difficile infection. Clin Gastroenterol Hepatol 8: 471-473.
72. Burns DA, Heap JT, Minton NP (2010) Clostridium difficile spore germination: an update. Res Microbiol 161: 730-734.
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.
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).
75. El-Matary W, Simpson R, Ricketts-Burns N (2012) Fecal microbiota transplantation: are we opening a can of worms? Gastroenterology 143: e19-e20.
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: 994-1002.
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).
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).
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: 23041678.
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: 761-767.
81. Metchnikoff E, Mitchell PCS (1907) The prolongation of life: optimistic studies. William Heinemann, London.