Fecal microbiota transplantation in metabolic syndrome: History, present and future

Gut Microbes

Volumn 8, Issue 3, 2017, Pages 253-267

  de Groot, P F ^a   Frissen, M N ^a   de Clercq, N C ^a   Nieuwdorp, M ^a,b,c  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

fecal transplantation; metabolic syndrome; microbiota

Indexed keywords

ALBUMIN; FIDAXOMICIN; METRONIDAZOLE; VANCOMYCIN;

ACIDOSIS; ADULT; AGED; ARTIFICIAL VENTILATION; CLINICAL ARTICLE; CLOSTRIDIUM DIFFICILE INFECTION; COLON RESECTION; COMPARATIVE STUDY; DISEASE SEVERITY; FECAL MICROBIOTA TRANSPLANTATION; FECES MICROFLORA; FEMALE; FEVER; HUMAN; HYPOTENSION; HYPOVOLEMIC SHOCK; ILEUS; LENGTH OF STAY; LEUKOCYTE COUNT; MALE; MENTAL DISEASE; MIDDLE AGED; OUTCOME ASSESSMENT; OVERALL SURVIVAL; REVIEW; RISK FACTOR; SEPTIC SHOCK; TOXIC MEGACOLON; VERY ELDERLY; ANIMAL; ATHEROSCLEROSIS; CLOSTRIDIUM INFECTION; DISEASE MODEL; FECES; HOST PATHOGEN INTERACTION; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INSULIN RESISTANCE; INTESTINE; INTESTINE FLORA; METABOLIC SYNDROME X; MICROBIOLOGY; NONALCOHOLIC FATTY LIVER; RANDOMIZED CONTROLLED TRIAL (TOPIC); TRENDS;

ANIMALS; ATHEROSCLEROSIS; CLOSTRIDIUM INFECTIONS; DISEASE MODELS, ANIMAL; FECAL MICROBIOTA TRANSPLANTATION; FECES; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INSULIN RESISTANCE; INTESTINES; METABOLIC SYNDROME; NON-ALCOHOLIC FATTY LIVER DISEASE; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 85020505801     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2017.1293224     Document Type: Review

References (111)

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 [Internet] 2012 [cited 2015Feb13]; 107:1755; author reply p.1755-p.6. Available from:http://dx.doi.org/10.1038/ajg.2012.251; PMID:23160295; http://dx.doi.org/10.1038/ajg.2012.251
2. Gerke H. “Fecal Transplantation.” Health at Iowa. University of Iowa Health Care [Internet] 2014; Available from:http://medcom.uiowa.edu/health/fecal-transplantation/
3. Uwlfoh SS, Dgglwlrqdo RU, Derxw L, Duwlfoh W, Lewin RA. More on Merde. 2016
4. Tetro JA. Applications of Fecal Microbiota Transplantation - The Human Microbiome Handbook. 2016
5. Merde:Excursions in Scientific, Cultural, and Socio-Historical Coprology:Ralph A. Lewin:9780812992519:Amazon.com:Books [Internet]. [cited 2015Feb15]; Available from:http://www.amazon.com/Merde-Excursions-Scientific-Socio-Historical-Coprology/dp/0812992512
6. Shanahan F. The Ungloved Gut Hektoen International - A Journal of Medical Humanities - Hektoen Institute of Medicine. 2016
7. Anukam K, Reid G. Probiotics:100 years (1907–2007) after Elie Metchnikoff's Observation. Commun Curr Res Educ Top trends Appl Microbiol 2007; 466-74
8. Schultz M. Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflamm Bowel Dis [Internet] 2008 [cited 2017Jan9]; 14:1012-8. Available from:http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00054725-200807000-00017; PMID:18240278; http://dx.doi.org/10.1002/ibd.20377
9. DeSalle R. The Great Camel Dung Mystery - welcome to the microbiome. 2015
10. Yong E. Sham Poo Washes Out - The Atlantic - Atlantic Media Company. 2016
11. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery [Internet] 1958 [cited 2016Sep16]; 44:854-9. Available from:http://www.ncbi.nlm.nih.gov/pubmed/13592638 PMID:13592638
12. Bowden TA, Mansberger AR, Lykins LE. Pseudomembraneous enterocolitis:mechanism for restoring floral homeostasis. Am Surg [Internet] 1981 [cited 2016Sep16]; 47:178-83. Available from:http://www.ncbi.nlm.nih.gov/pubmed/7224366; PMID:7224366
13. Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med [Internet] 1978 [cited 2016Sep16]; 298:531-4. Available from:http://www.ncbi.nlm.nih.gov/pubmed/625309; PMID:625309; http://dx.doi.org/10.1056/NEJM197803092981003
14. Borody TJ, Paramsothy S, Agrawal G. Fecal microbiota transplantation:Indications, methods, evidence, and future directions. Curr Gastroenterol Rep 2013; 15:1-7; http://dx.doi.org/10.1007/s11894-013-0337-1
15. 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 [Internet] 1989 [cited 2016Sep12]; 150:604. Available from:http://www.ncbi.nlm.nih.gov/pubmed/2783214; PMID:2783214
16. Bennet J, Brinkman M. Treatment of Ulcerative Colitis By Implantation of Normal Colonic Flora. Lancet 1989; 333:164; http://dx.doi.org/10.1016/S0140-6736(89)91183-5
17. Andrews PJ, Borody TJ. “Putting back the bugs:” Bacterial treatment relieves chronic constipation and symptoms of irritable bowel syndrome [7].Med. J Aust 1993; 159:633-4
18. 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:A randomized trial. Ann Intern Med 2016; 165(9):609-616:1–9; PMID:27547925; http://dx.doi.org/10.7326/M16-0271
19. Cammarota G, Masucci L, Ianiro G, Bibbò S, Dinoi G, Costamagna G, Sanguinetti M, Gasbarrini A. Randomised clinical trial:faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection. Aliment Pharmacol Ther 2015; 41(9):835-43; PMID:25728808; http://dx.doi.org/10.1111/apt.13144
20. 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 [Internet] 2013; 368:407-15. Available from:http://dx.doi.org/10.1056/NEJMoa1205037; PMID:23323867; http://dx.doi.org/10.1056/NEJMoa1205037
21. Grehan MJ, Borody TJ, Leis SM, Campbell J, Mitchell H, Wettstein A. Durable alteration of the colonic microbiota by the administration of donor fecal flora. J Clin Gastroenterol 2010; 44:551-61; PMID:20716985; http://dx.doi.org/10.1097/MCG.0b013e3181e5d06b
22. 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; 107:1079-87; PMID:22450732; http://dx.doi.org/10.1038/ajg.2012.60
23. 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 [Internet] 2012 [cited 2015Jan15]; 107:1079-87. Available from:https://c6-qzr6satum-7fsf.sec.amc.nl/ajg/journal/v107/n7/full/ajg201260a.html; PMID:22450732; http://dx.doi.org/10.1038/ajg.2012.60
24. Agrawal M, Aroniadis OC, Brandt LJ, Kelly C, Freeman S, Surawicz C, Broussard E, Stollman N, Giovanelli A, Smith B, et al. The long-term efficacy and safety of fecal microbiota transplant for recurrent, severe, and complicated clostridium difficile infection in 146 elderly individuals. J Clin Gastroenterol 2016; 50:403-7; PMID:26352106
25. Mandalia A, Ward A, Tauxe W, Kraft CS, Dhere T. Fecal transplant is as effective and safe in immunocompromised as non-immunocompromised patients for Clostridium difficile. Int J Colorectal Dis [Internet] 2016 [cited 2016Sep16]; 31:1059-60. Available from:http://www.ncbi.nlm.nih.gov/pubmed/26410257; PMID:26410257; http://dx.doi.org/10.1007/s00384-015-2396-2
26. Ananthaswamy A. Bugs from your gut to mine. New Sci 2008; 209:8-9; http://dx.doi.org/10.1016/S0262-4079(08)62088-6
27. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science [Internet] 2013 [cited 2017Jan9]; 339:548-54. Available from:http://www.sciencemag.org/cgi/doi/10.1126/science.1229000; PMID:23363771; http://dx.doi.org/10.1126/science.1229000
28. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, et al. Gut Microbiomes of Malawian Twin. Science (80-) 2013; 339(6119):548; http://dx.doi.org/10.1126/science.1229000
29. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci 2007; 104:979-84; PMID:17210919; http://dx.doi.org/10.1073/pnas.0605374104
30. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature [Internet] 2006 [cited 2014Jul10]; 444:1027-31. Available from:http://www.ncbi.nlm.nih.gov/pubmed/17183312; PMID:17183312; http://dx.doi.org/10.1038/nature05414
31. Bäckhed F, Ding H, Wang T, Hooper L V, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A [Internet] 2004 [cited 2016Aug26]; 101:15718-23. Available from:http://www.ncbi.nlm.nih.gov/pubmed/15505215; PMID:15505215; http://dx.doi.org/10.1073/pnas.0407076101
32. Kulecka M, Paziewska A, Zeber-Lubecka N, Ambrozkiewicz F, Kopczynski M, Kuklinska U, Pysniak K, Gajewska M, Mikula M, Ostrowski J. Prolonged transfer of feces from the lean mice modulates gut microbiota in obese mice. Nutr Metab (Lond) 2016; 13:57; PMID:27559357; http://dx.doi.org/10.1186/s12986-016-0116-8
33. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005; 102:11070-5; PMID:16033867; http://dx.doi.org/10.1073/pnas.0504978102
34. Di Luccia B, Crescenzo R, Mazzoli A, Cigliano L, Venditti P, Walser JC, Widmer A, Baccigalupi L, Ricca E, Iossa S. Rescue of fructose-induced metabolic syndrome by antibiotics or faecal transplantation in a rat model of obesity. PLoS One 2015; 10:1-19; http://dx.doi.org/10.1371/journal.pone.0134893
35. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013; 341:1241214; PMID:24009397; http://dx.doi.org/10.1126/science.1241214
36. Liou AP, Paziuk M, Luevano J-M, Machineni S, Turnbaugh PJ, Kaplan LM. Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med [Internet] 2013 [cited 2014Sep30]; 5:178ra41. Available from:http://stm.sciencemag.org/content/5/178/178ra41.long; PMID:23536013; http://dx.doi.org/10.1126/scitranslmed.3005687
37. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. Enterotypes of the human gut microbiome. Nature [Internet] 2011 [cited 2016Sep2]; 473:174-80. Available from:http://www.ncbi.nlm.nih.gov/pubmed/21508958; PMID:21508958; http://dx.doi.org/10.1038/nature09944
38. Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B, Nielsen J, Bäckhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature [Internet] 2013 [cited 2014Jul9]; 498:99-103. Available from:https://c6-qzr6satum-7fsf.sec.amc.nl/nature/journal/v498/n7452/full/nature12198.html; PMID:23719380; http://dx.doi.org/10.1038/nature12198
39. Alang N, Kelly CR. Weight gain after fecal microbiota transplantation. Open forum Infect Dis [Internet] 2015 [cited 2016Sep16]; 2:ofv004. Available from:http://www.ncbi.nlm.nih.gov/pubmed/26034755; PMID:26034755; http://dx.doi.org/10.1093/ofid/ofv004
40. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JFWM, 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 [Internet] 2012 [cited 2014Jul9]; 143:913-6.e7. Available from:http://www.sciencedirect.com/science/article/pii/S001650851200892X; PMID:22728514; http://dx.doi.org/10.1053/j.gastro.2012.06.031
41. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha:direct role in obesity-linked insulin resistance. Science [Internet] 1993 [cited 2016Sep5]; 259:87-91. Available from:http://www.ncbi.nlm.nih.gov/pubmed/7678183; PMID:7678183; http://dx.doi.org/10.1126/science.7678183
42. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest [Internet] 2006 [cited 2014Nov12]; 116:1793-801. Available from:/pmc/articles/PMC1483173/?report=abstract; PMID:16823477; http://dx.doi.org/10.1172/JCI29069
43. Hirosumi J, Tuncman G, Chang L, Görgün CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature [Internet] 2002 [cited 2016Sep13]; 420:333-6. Available from:http://www.ncbi.nlm.nih.gov/pubmed/12447443; PMID:12447443; http://dx.doi.org/10.1038/nature01137
44. Özcan U, Cao Q, Yilmaz E, Lee A-H, Iwakoshi NN, Özdelen E, Tuncman G, Görgün C, Glimcher LH, Hotamisligil GS. Endoplasmic Reticulum Stress Links Obesity, Insulin Action, and Type 2 Diabetes. Science (80-) 2004; 306:457-61; http://dx.doi.org/10.1126/science.1103160
45. Copps KD, White MF. Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia [Internet] 2012 [cited 2016Sep15]; 55:2565-82. Available from:http://www.ncbi.nlm.nih.gov/pubmed/22869320; PMID:22869320; http://dx.doi.org/10.1007/s00125-012-2644-8
46. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science [Internet] 2001 [cited 2016Sep15]; 292:104-6. Available from:http://www.ncbi.nlm.nih.gov/pubmed/11292874; PMID:11292874; http://dx.doi.org/10.1126/science.1057991
47. Selman C, Lingard S, Choudhury AI, Batterham RL, Claret M, Clements M, Ramadani F, Okkenhaug K, Schuster E, Blanc E, et al. Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J [Internet] 2008 [cited 2016Sep15]; 22:807-18. Available from:http://www.ncbi.nlm.nih.gov/pubmed/17928362; PMID:17928362; http://dx.doi.org/10.1096/fj.07-9261com
48. Tontonoz P, Spiegelman BM. Fat and Beyond:The Diverse Biology of PPARγ. Annu Rev Biochem [Internet] 2008 [cited 2017Jan2]; 77:289-312. Available from:http://www.ncbi.nlm.nih.gov/pubmed/18518822; PMID:18518822; http://dx.doi.org/10.1146/annurev.biochem.77.061307.091829
49. Zelvyte I, Dominaitiene R, Crisby M, Janciauskiene S. Modulation of inflammatory mediators and pparγand nfκb expression by pravastatin in response to lipoproteins in human monocytes in vitro. Pharmacol Res [Internet] 2002 [cited 2017Jan2]; 45:147-54. Available from:http://www.ncbi.nlm.nih.gov/pubmed/11846628; PMID:11846628; http://dx.doi.org/10.1006/phrs.2001.0922
50. Piya MK, Harte AL, McTernan PG. Metabolic endotoxaemia:is it more than just a gut feeling? Curr Opin Lipidol [Internet] 2013 [cited 2016Sep8]; 24:78-85. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23298961; PMID:23298961; http://dx.doi.org/10.1097/MOL.0b013e32835b4431
51. Bester J, Soma P, Kell DB, Pretorius E. Viscoelastic and ultrastructural characteristics of whole blood and plasma in Alzheimer-type dementia, and the possible role of bacterial lipopolysaccharides (LPS). Oncotarget [Internet] 2015 [cited 2016Sep9]; 6:35284-303. Available from:http://www.ncbi.nlm.nih.gov/pubmed/26462180; PMID:26462180
52. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest [Internet] 2006 [cited 2016Sep6]; 116:1793-801. Available from:http://www.ncbi.nlm.nih.gov/pubmed/16823477; PMID:16823477; http://dx.doi.org/10.1172/JCI29069
53. Koren O, Spor A, Felin J, Fåk F, Stombaugh J, Tremaroli V, Behre CJ, Knight R, Fagerberg B, Ley RE, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci U S A [Internet] 2011; 108 [cited 2016Sep5]:4592-8. Available from:http://www.ncbi.nlm.nih.gov/pubmed/20937873; PMID:20937873; http://dx.doi.org/10.1073/pnas.1011383107
54. Zulian A, Cancello R, Ruocco C, Gentilini D, Di Blasio AM, Danelli P, Micheletto G, Cesana E, Invitti C. Differences in visceral fat and fat bacterial colonization between ulcerative colitis and Crohn's disease. An in vivo and in vitro study. PLoS One [Internet] 2013 [cited 2016Sep7]; 8:e78495. Available from:http://www.ncbi.nlm.nih.gov/pubmed/24205244; PMID:24205244; http://dx.doi.org/10.1371/journal.pone.0078495
55. McGuckin MA, Lindén SK, Sutton P, Florin TH. Mucin dynamics and enteric pathogens. Nat Rev Microbiol [Internet] 2011 [cited 2016Sep7]; 9:265-78. Available from:http://www.ncbi.nlm.nih.gov/pubmed/21407243; PMID:21407243; http://dx.doi.org/10.1038/nrmicro2538
56. Quigley EMM. Leaky gut–concept or clinical entity? Curr Opin Gastroenterol [Internet] 2016 [cited 2016Sep7]; 32:74-9. Available from:http://content.wkhealth.com/linkback/openurl?sid = WKPTLP:landingpage&an = 00001574-201603000-00004; PMID:26760399; http://dx.doi.org/10.1097/MOG.0000000000000243
57. Grootjans J, Thuijls G, Verdam F, Derikx JP, Lenaerts K, Buurman WA. Non-invasive assessment of barrier integrity and function of the human gut. World J Gastrointest Surg [Internet] 2010 [cited 2016Sep7]; 2:61-9. Available from:http://www.ncbi.nlm.nih.gov/pubmed/21160852; PMID:21160852; http://dx.doi.org/10.4240/wjgs.v2.i3.61
58. Maxton DG, Bjarnason I, Reynolds AP, Catt SD, Peters TJ, Menzies IS. Lactulose, 51Cr-labelled ethylenediaminetetra-acetate, L-rhamnose and polyethyleneglycol 400 [corrected] as probe markers for assessment in vivo of human intestinal permeability. Clin Sci (Lond) [Internet] 1986 [cited 2017Jan3]; 71:71-80. Available from:http://www.ncbi.nlm.nih.gov/pubmed/3086024; PMID:3086024; http://dx.doi.org/10.1042/cs0710071
59. Wu L-L, Peng W-H, Kuo W-T, Huang C-Y, Ni Y-H, Lu K-S, Turner JR, Yu LCH. Commensal bacterial endocytosis in epithelial cells is dependent on myosin light chain kinase-activated brush border fanning by interferon-γ. Am J Pathol [Internet] 2014 [cited 2016Sep7]; 184:2260-74. Available from:http://www.ncbi.nlm.nih.gov/pubmed/24911373; PMID:24911373; http://dx.doi.org/10.1016/j.ajpath.2014.05.003
60. Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A, et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell [Internet] 2016 [cited 2016Nov18]; 167:1339-1353.e21. Available from:http://linkinghub.elsevier.com/retrieve/pii/S0092867416314647; PMID:27863247; http://dx.doi.org/10.1016/j.cell.2016.10.043
61. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes [Internet] 2007 [cited 2016Sep7]; 56:1761-72. Available from:http://www.ncbi.nlm.nih.gov/pubmed/17456850; PMID:17456850; http://dx.doi.org/10.2337/db06-1491
62. Munford RS. Endotoxemia-menace, marker, or mistake? J Leukoc Biol [Internet] 2016 [cited 2016Sep7]; Available from:http://www.ncbi.nlm.nih.gov/pubmed/27418356; PMID:27418356
63. Lu M, Munford RS. The transport and inactivation kinetics of bacterial lipopolysaccharide influence its immunological potency in vivo. J Immunol [Internet] 2011 [cited 2016Sep7]; 187:3314-20. Available from:http://www.ncbi.nlm.nih.gov/pubmed/21849675; PMID:21849675; http://dx.doi.org/10.4049/jimmunol.1004087
64. Olofsson P, Nylander G, Olsson P. Endotoxin:routes of transport in experimental peritonitis. Am J Surg [Internet] 1986 [cited 2016Sep7]; 151:443-6. Available from:http://www.ncbi.nlm.nih.gov/pubmed/3963300; PMID:3963300; http://dx.doi.org/10.1016/0002-9610(86)90098-X
65. Cindoruk M, Cirak MY, Unal S, Karakan T, Erkan G, Engin D, Dumlu S, Turet S. Identification of Helicobacter species by 16S rDNA PCR and sequence analysis in human liver samples from patients with various etiologies of benign liver diseases. Eur J Gastroenterol Hepatol [Internet] 2008 [cited 2016Sep8]; 20:33-6. Available from:http://www.ncbi.nlm.nih.gov/pubmed/18090988; PMID:18090988; http://dx.doi.org/10.1097/MEG.0b013e3282efa4f2
66. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud D-J, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res [Internet] 2013 [cited 2014Nov17]; 54:2325-40. Available from:http://www.jlr.org/content/54/9/2325.long; PMID:23821742; http://dx.doi.org/10.1194/jlr.R036012
67. Canfora EE, Jocken JW, Blaak EE. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat Rev Endocrinol [Internet] 2015 [cited 2016Sep13]; 11:577-91. Available from:http://www.nature.com/doifinder/10.1038/nrendo.2015.128; PMID:26260141; http://dx.doi.org/10.1038/nrendo.2015.128
68. Wang H-B, Wang P-Y, Wang X, Wan Y-L, Liu Y-C. Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein Claudin-1 transcription. Dig Dis Sci [Internet] 2012 [cited 2016Jun6]; 57:3126-35. Available from:http://www.ncbi.nlm.nih.gov/pubmed/22684624; PMID:22684624; http://dx.doi.org/10.1007/s10620-012-2259-4
69. Zimmerman MA, Singh N, Martin PM, Thangaraju M, Ganapathy V, Waller JL, Shi H, Robertson KD, Munn DH, Liu K. Butyrate suppresses colonic inflammation through HDAC1-dependent Fas upregulation and Fas-mediated apoptosis of T cells. Am J Physiol Gastrointest Liver Physiol [Internet] 2012 [cited 2016Sep5]; 302:G1405-15. Available from:http://www.ncbi.nlm.nih.gov/pubmed/22517765; PMID:22517765; http://dx.doi.org/10.1152/ajpgi.00543.2011
70. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Bäckhed F, Mithieux G. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell [Internet] 2014 [cited 2016Apr15]; 156:84-96. Available from:http://www.sciencedirect.com/science/article/pii/S009286741301550X; PMID:24412651; http://dx.doi.org/10.1016/j.cell.2013.12.016
71. Freeland KR, Wolever TMS. Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-alpha. Br J Nutr [Internet] 2010 [cited 2016Sep5]; 103:460-6. Available from:http://www.ncbi.nlm.nih.gov/pubmed/19818198; PMID:19818198; http://dx.doi.org/10.1017/S0007114509991863
72. Todesco T, Rao A V, Bosello O, Jenkins DJ. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am J Clin Nutr [Internet] 1991 [cited 2016Sep5]; 54:860-5. Available from:http://www.ncbi.nlm.nih.gov/pubmed/1951157; PMID:1951157
73. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009; 58:1509-17; PMID:19366864; http://dx.doi.org/10.2337/db08-1637
74. Wahlström A, Sayin SI, Marschall H-U, Bäckhed F. Intestinal Crosstalk between Bile acids and microbiota and its impact on host metabolism. Cell Metab 2016; 24(1):41-50; PMID:27320064; http://dx.doi.org/10.1016/j.cmet.2016.05.005
75. Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T, Jensen BAH, Forslund K, Hildebrand F, Prifti E, Falony G, et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature [Internet] 2016 [cited 2016Sep5]; 535:376-81. Available from:http://www.ncbi.nlm.nih.gov/pubmed/27409811; PMID:27409811; http://dx.doi.org/10.1038/nature18646
76. Shin N-R, Lee J-C, Lee H-Y, Kim M-S, Whon TW, Lee M-S, Bae J-W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut [Internet] 2014 [cited 2015Mar5]; 63:727-35. Available from:https://c6-axo6gmj-8jj.sec.amc.nl/content/63/5/727.full; PMID:23804561; http://dx.doi.org/10.1136/gutjnl-2012-303839
77. Li J, Lin S, Vanhoutte PM, Woo CW, Xu A. Akkermansia Muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe−/− Mice. Circulation [Internet] 2016 [cited 2016Sep5]; 133:2434-46. Available from:http://www.ncbi.nlm.nih.gov/pubmed/27143680; PMID:27143680; http://dx.doi.org/10.1161/CIRCULATIONAHA.115.019645
78. Nadal I, Donat E, Donant E, Ribes-Koninckx C, Calabuig M, Sanz Y. Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J Med Microbiol [Internet] 2007 [cited 2015Nov14]; 56:1669-74. Available from:http://jmm.microbiologyresearch.org/content/journal/jmm/10.1099/jmm.0.47410-0; PMID:18033837; http://dx.doi.org/10.1099/jmm.0.47410-0
79. Wiedermann CJ, Kiechl S, Dunzendorfer S, Schratzberger P, Egger G, Oberhollenzer F, Willeit J. Association of endotoxemia with carotid atherosclerosis and cardiovascular disease:prospective results from the Bruneck Study. J Am Coll Cardiol [Internet] 1999 [cited 2016Aug26]; 34:1975-81. Available from:http://www.ncbi.nlm.nih.gov/pubmed/10588212; PMID:10588212; http://dx.doi.org/10.1016/S0735-1097(99)00448-9
80. Spence JD. Effects of the Intestinal Microbiome on Constituents of Red Meat and Egg Yolks:A New Window Opens on Nutrition and Cardiovascular Disease. Can J Cardiol 2014; 30:150-1; PMID:24461914; http://dx.doi.org/10.1016/j.cjca.2013.11.019
81. Karlsson FH, Fåk F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, Bäckhed F, Nielsen J. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun [Internet] 2012 [cited 2016Sep6]; 3:1245. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23212374; PMID:23212374; http://dx.doi.org/10.1038/ncomms2266
82. Tang WHW, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med [Internet] 2013 [cited 2016Sep5]; 368:1575-84. Available from:http://www.nejm.org/doi/abs/10.1056/NEJMoa1109400; PMID:23614584; http://dx.doi.org/10.1056/NEJMoa1109400
83. Zhu W, Gregory JC, Org E, Buffa JA, Gupta N, Wang Z, Li L, Fu X, Wu Y, Mehrabian M, et al. Gut Microbial Metabolite TMAO enhances platelet hyperreactivity and thrombosis risk. Cell [Internet] 2016 [cited 2016Sep6]; 165:111-24. Available from:http://www.ncbi.nlm.nih.gov/pubmed/26972052; PMID:26972052; http://dx.doi.org/10.1016/j.cell.2016.02.011
84. Chan YK, El-Nezami H, Chen Y, Kinnunen K, Kirjavainen P V. Probiotic mixture VSL#3 reduce high fat diet induced vascular inflammation and atherosclerosis in ApoE(−/−) mice. AMB Express [Internet] 2016 [cited 2016Sep5]; 6:61. Available from:http://www.ncbi.nlm.nih.gov/pubmed/27576894; PMID:27576894; http://dx.doi.org/10.1186/s13568-016-0229-5
85. Karbach SH, Schönfelder T, Brandão I, Wilms E, Hörmann N, Jäckel S, Schüler R, Finger S, Knorr M, Lagrange J, et al. Gut microbiota promote angiotensin II-induced arterial hypertension and vascular Dysfunction. J Am Heart Assoc [Internet] 2016 [cited 2016Sep6]; 5. Available from:http://www.ncbi.nlm.nih.gov/pubmed/27577581; PMID:27577581; http://dx.doi.org/10.1161/JAHA.116.003698
86. Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, Gill SR. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients:a connection between endogenous alcohol and NASH. Hepatology [Internet] 2013 [cited 2016Sep13]; 57:601-9. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23055155; PMID:23055155; http://dx.doi.org/10.1002/hep.26093
87. Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol [Internet] 2013 [cited 2016Sep13]; 11:868-75-3. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23454028; http://dx.doi.org/10.1016/j.cgh.2013.02.015
88. Mouzaki M, Comelli EM, Arendt BM, Bonengel J, Fung SK, Fischer SE, McGilvray ID, Allard JP. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology [Internet] 2013 [cited 2016Sep13]; 58:120-7. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23401313; PMID:23401313; http://dx.doi.org/10.1002/hep.26319
89. Ruiz AG, Casafont F, Crespo J, Cayón A, Mayorga M, Estebanez A, Fernadez-Escalante JC, Pons-Romero F. Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients:evidence for the potential role of endotoxin in the pathogenesis of non-alcoholic steatohepatitis. Obes Surg [Internet] 2007 [cited 2016Sep6]; 17:1374-80. Available from:http://www.ncbi.nlm.nih.gov/pubmed/18000721; PMID:18000721; http://dx.doi.org/10.1007/s11695-007-9243-7
90. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, Mascianà R, Forgione A, Gabrieli ML, Perotti G, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology [Internet] 2009 [cited 2016Sep6]; 49:1877-87. Available from:http://www.ncbi.nlm.nih.gov/pubmed/19291785; PMID:19291785; http://dx.doi.org/10.1002/hep.22848
91. Bergheim I, Weber S, Vos M, Krämer S, Volynets V, Kaserouni S, McClain CJ, Bischoff SC. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice:role of endotoxin. J Hepatol [Internet] 2008 [cited 2016Sep6]; 48:983-92. Available from:http://www.ncbi.nlm.nih.gov/pubmed/18395289; PMID:18395289; http://dx.doi.org/10.1016/j.jhep.2008.01.035
92. Cano PG, Santacruz A, Trejo FM, Sanz Y. Bifidobacterium CECT 7765 improves metabolic and immunological alterations associated with obesity in high-fat diet-fed mice. Obesity (Silver Spring) [Internet] 2013 [cited 2016Sep13]; 21:2310-21. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23418126; PMID:23418126; http://dx.doi.org/10.1002/oby.20330
93. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, Thaiss CA, Kau AL, Eisenbarth SC, Jurczak MJ, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature [Internet] 2012 [cited 2016Aug26]; 482:179-85. Available from:http://www.ncbi.nlm.nih.gov/pubmed/22297845; PMID:22297845
94. Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut [Internet] 2013 [cited 2016Sep13]; 62:1787-94. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23197411; PMID:23197411; http://dx.doi.org/10.1136/gutjnl-2012-303816
95. Wong VW-S, Won GL-H, Chim AM-L, Chu WC-W, Yeung DK-W, Li KC-T, Chan HL-Y. Treatment of nonalcoholic steatohepatitis with probiotics. A proof-of-concept study. Ann Hepatol [Internet] [cited 2016Sep13]; 12:256-62. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23396737; PMID:23396737
96. Bjarnason I, Peters TJ, Wise RJ. The leaky gut of alcoholism:possible route of entry for toxic compounds. Lancet (London, England) [Internet] 1984 [cited 2016Sep6]; 1:179-82. Available from:http://www.ncbi.nlm.nih.gov/pubmed/6141332; PMID:6141332; http://dx.doi.org/10.1016/S0140-6736(84)92109-3
97. Moschen AR, Kaser S, Tilg H. Non-alcoholic steatohepatitis:a microbiota-driven disease. Trends Endocrinol Metab [Internet] 2013 [cited 2016Sep6]; 24:537-45. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23827477; PMID:23827477; http://dx.doi.org/10.1016/j.tem.2013.05.009
98. Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, et al. Gut dysbiosis is linked to hypertension. Hypertens (Dallas, Tex 1979) [Internet] 2015 [cited 2016Sep7]; 65:1331-40. Available from:http://www.ncbi.nlm.nih.gov/pubmed/25870193; http://dx.doi.org/10.1161/HYPERTENSIONAHA.115.05315
99. Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A, Han J, Brunet I, Wan L-X, Rey F, Wang T, et al. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Natl Acad Sci U S A [Internet] 2013 [cited 2016Sep7]; 110:4410-5. Available from:http://www.ncbi.nlm.nih.gov/pubmed/23401498; PMID:23401498; http://dx.doi.org/10.1073/pnas.1215927110
100. Li SS, Zhu A, Benes V, Costea PI, Hercog R, Hildebrand F, Huerta-Cepas J, Nieuwdorp M, Salojarvi J, Voigt AY, et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science (80-) [Internet] 2016 [cited 2016Apr29]; 352:586-9. Available from:http://www.ncbi.nlm.nih.gov/pubmed/27126044; http://dx.doi.org/10.1126/science.aad8852
101. Smits LP, Bouter KEC, de Vos WM, Borody TJ, Nieuwdorp M. Therapeutic potential of fecal microbiota transplantation. Gastroenterology [Internet] 2013 [cited 2014Nov18]; 145:946-53. Available from:http://www.sciencedirect.com/science/article/pii/S0016508513012791; PMID:24018052;http://dx.doi.org/10.1053/j.gastro.2013.08.058
102. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, Goulding D, Lawley TD. Culturing of “unculturable” human microbiota reveals novel taxa and extensive sporulation. Nature [Internet] 2016 [cited 2016May4]; 533:543-6. Available from:http://www.nature.com/nature/journal/v533/n7604/full/nature17645.html?WT.ec_id=NATURE-20160526&spMailingID=51458273&spUserID=NTMxMjc2MzUyNDYS1&spJobID =923132954&spReportId =OTIzMTMyOTU0S0; PMID:27144353; http://dx.doi.org/10.1038/nature17645
103. De Vos WM. Fame and future of faecal transplantations - developing next-generation therapies with synthetic microbiomes. Microb Biotechnol 2013; 6:316-25; PMID:23574632; http://dx.doi.org/10.1111/1751-7915.12047
104. 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; 352:586-9; PMID:27126044; http://dx.doi.org/10.1126/science.aad8852
105. Robins-browne RM, Levine M, Path FF. The fate of ingested in the proximal small intestine. Am J Clin Nut 1981; 34(4):514-9
106. Seedorf H, Griffin NW, Ridaura VK, Reyes A, Cheng J, Rey FE, Smith MI, Simon GM, Scheffrahn RH, Woebken D, et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 2014; 159:253-66; PMID:25284151; http://dx.doi.org/10.1016/j.cell.2014.09.008
107. Kahn SA, Gorawara-Bhat R, Rubin DT. Fecal bacteriotherapy for ulcerative colitis:Patients are ready, are we? Inflamm Bowel Dis 2012; 18:676-84; PMID:21618362; http://dx.doi.org/10.1002/ibd.21775
108. Khan MT, Nieuwdorp M, Bäckhed F. Microbial modulation of insulin sensitivity. Cell Metab [Internet] 2014 [cited 2015Jan7]; 20:753-60. Available from:http://www.sciencedirect.com/science/article/pii/S1550413114003143; PMID:25176147; http://dx.doi.org/10.1016/j.cmet.2014.07.006
109. 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; 149:223-37; PMID:25982290; http://dx.doi.org/10.1053/j.gastro.2015.05.008
110. Zmora N, Zeevi D, Korem T, Segal E, Elinav E. Taking it personally:Personalized utilization of the human microbiome in health and disease. Cell Host Microbe 2016; 19:12-20; PMID:26764593; http://dx.doi.org/10.1016/j.chom.2015.12.016
111. Zeevi D, Korem T, Zmora N, Israeli D, Rothschild D, Weinberger A, Ben-Yacov O, Lador D, Avnit-Sagi T, Lotan-Pompan M, et al. Personalized nutrition by prediction of glycemic responses. Cell [Internet] 2015 [cited 2015Nov19]; 163:1079-94. Available from:http://www.ncbi.nlm.nih.gov/pubmed/26590418; PMID:26590418;http://dx.doi.org/10.1016/j.cell.2015.11.001