862
Views
0
CrossRef citations to date
0
Altmetric
Review

Role of Altered Intestinal Microbiota in Systemic Inflammation and Cardiovascular Disease in Chronic Kidney Disease

, , , , &
Pages 399-410 | Published online: 24 Apr 2014

References

  • Siasos G , TousoulisD , MichaleaSet al. Biomarkers determining cardiovascular risk in patients with kidney disease . Curr. Med. Chem.19 ( 16 ), 2555 – 2571 ( 2012 ).
  • Stenvinkel P . Inflammation as a target for improving health in chronic kidney disease . F1000 Med. Rep.17 , 2 – 88 ( 2010 ).
  • Schepers E , MeertN , GlorieuxGet al. P- Cresylsulphate, the main in vivo metabolite of p-cresol, activates leucocyte free radical production . Nephrol. Dial. Transplant.22 , 592 – 596 ( 2007 ).
  • Musso G , GambinoR , CassaderM . Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes . Annu. Rev. Med.62 , 361 – 380 ( 2011 ).
  • Vaziri ND , WongJ , PahlMet al. Chronic kidney disease alters intestinal microbial flora . Kidney Int.83 ( 2 ), 308 – 315 ( 2013 ).
  • Tremaroli V , BäckhedF . Functional interactions between the gut microbiota and host metabolism . Nature13, 489 ( 7415 ), 242 – 249 ( 2013 ).
  • Vaziri ND . CKD impairs barrier function and alters microbial flora of the intestine: a major link to inflammation and uremic toxicity . Curr. Opin. Nephrol. Hyperten.21 , 587 – 592 ( 2012 ).
  • Vaziri ND , YuanJ , RahimiA , NiZ , SaidH , SubramanianVS . Disintegration of colonic epithelial tight junction in uremia: a likely cause of CKD-associated inflammation . Nephrol. Dial. Transplant.27 ( 7 ), 2686 – 2693 ( 2012 ).
  • Eckburg PB , BikEM , BernsteinCNet al. Diversity of the human intestinal microbial flora . Science308 , 1635 – 1168 ( 2005 ).
  • Cani PD , DelzenneNM . The role of the gut microbiota in energy metabolism and metabolic disease . Curr. Pharm. Des.15 , 1546 – 1558 ( 2009 ).
  • Sanz Y , NadalI , SanchezE . Probiotics as drugs against human gastrointestinal infections . Recent Pat. Antiinfect. Drug Discov.2 , 148 – 156 ( 2007 ).
  • Medina M , IzquierdoE , EnnaharSet al. Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications . Clin. Exp. Im.150 ( 3 ), 531 – 538 ( 2007 ).
  • Hylemon PB , ZhouH , PandakWMet al. Bile acids as regulatory molecules . J. Lipid. Res.50 , 1509 – 1520 ( 2009 ).
  • Prawitt J , AbdelkarimM , StroeveJHet al. Farnesoid X receptor deficiency improves glucose homeostasis in mouse models of obesity . Diabetes60 , 1861 – 1871 ( 2011 ).
  • Scott KP , GratzSW , SheridanPOet al. The influence of diet on the gut microbiota . Pharmacol. Res. 69(1), 52–60 ( 2012 ).
  • Maslowski KM , VieiraAT , NgAet al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 . Nature461 , 1282 – 1286 ( 2009 ).
  • Sina C , GavrilovaO , FörsterMet al. G protein-coupled receptor 43 is essential for neutrophil recruitment during intestinal inflammation . J. Immunol.183 , 7514 – 7522 ( 2009 ).
  • Tolhurst G , HeffronH , LamYSet al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2 . Diabetes61 , 364 – 371 ( 2012 ).
  • Smith PM , HowittMR , PanikovNet al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis . Science341 ( 6145 ), 569 – 573 ( 2013 ).
  • Lin HV , FrassettoA , KowalikEJJret al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms . PLoS ONE7 ( 4 ), 1 – 9 ( 2012 ).
  • Hara T , KimuraI , InoueDet al. Free fatty acid receptors and their role in regulation of energy metabolism . Rev. Physiol. Biochem. Pharmacol.164 , 77 – 116 ( 2013 ).
  • Pluznick JL , ProtzkoRJ , GevorgyanHet al. Olfactory receptor esponding to gut microbiota derived signals plays a role in renin secretion and blood pressure regulation . Proc. Natl Acad. Sci. USA110 ( 11 ), 4410 – 4415 ( 2013 ).
  • Brinkworth GD , NoakesM , CliftonPMet al. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations . Br. J. Nutr.101 , 1493 – 1502 ( 2009 ).
  • Laugerette F , FuretJP , DebardCet al. Oil composition of high-fat diet affects metabolic inflammation differently in connection with endotoxin receptors in mice . Am. J. Physiol. Endocrinol. Metab.302 ( 3 ), 374 – 386 ( 2012 ).
  • Hughes R , MageeEA , BinghamS . Protein degradation in the large intestine: Relevance to colorectal cancer . Curr. Issues Intest. Microbiol.1 , 51 – 58 ( 2000 ).
  • Davila AM , BlachierF , GottelandMet al. Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host . Pharmacol. Res.69 ( 1 ), 114 – 126 ( 2013 ).
  • Harris K , KassisA , MajorGet al. Is the gut microbiota a new factor contributing to obesity and its metabolic disorders? J. Obes. 8 , 79 – 151 ( 2012 ).
  • Howitt MR , GarrettWS . Gut microbiota and cardiovascular disease connectivity . Nat. Med.18 ( 8 ), 1188 – 1189 ( 2012 ).
  • Koeth RA , WangZ , LevisonBSet al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis . Nat. Med.19 ( 5 ), 576 – 585 ( 2013 ).
  • Wang Z , KlipfellE , BennettBJet al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease . Nature472 ( 7341 ), 57 – 63 ( 2011 ).
  • Manco M . Endotoxin as a missed link among all the metabolic abnormalities in the metabolic syndrome . Atherosclerosis206 , 36 ( 2011 ).
  • Ley RE , TurnbaughPJ , KleinSet al. Microbial ecology: human gut microbes associated with obesity . Nature444 , 1022 – 1023 ( 2006 ).
  • Marteau P . Bacterial flora in inflammatory bowel disease . Dig. Dis.27 , 99 – 103 ( 2009 ).
  • Koren O , GoodrichJK , CullenderTCet al. Host remodeling of the gut microbiome and metabolic changes during pregnancy . Cell150 ( 3 ), 470 – 480 ( 2012 ).
  • Konstantinov SR , vander Woude CJ , PeppelenboschMP . Do pregnancy-related changes in the microbiome stimulate innate immunity?Trends Mol. Med.19 ( 8 ), 454 – 459 ( 2013 ).
  • Turnbaugh PJ , HamadyM , YatsunenkoTet al. A core gut microbiome in obese and lean twins . Nature457 ( 7228 ), 480 – 484 ( 2009 ).
  • Cani PD , BibiloniR , KnaufCet al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice . Diabetes57 ( 6 ), 1470 – 1481 ( 2008 ).
  • Szeto CC , KwanBC , ChowKMet al. Endotoxemia is related to systemic inflammation and atherosclerosis in peritoneal dialysis patients . Clin. J. Am. Soc. Nephrol.3 , 431 – 436 ( 2008 ).
  • Cluny NL , ReimerRA , SharkeyKA . Cannabinoid signalling regulates inflammation and energy balance: the importance of the brain–gut axis . Brain Behav. Immun.26 ( 5 ), 691 – 698 ( 2012 ).
  • Matias I , CristinoL , DiMarzo . Endocannabinoids: some like it fat (and sweet too) . J. Neuroendocrinol.20 ( 1 ), 100 – 109 ( 2008 ).
  • Muccioli GG , NaslainD , BäckhedFet al. The endocannabinoid system links gut microbiota to adipogenesis . Mol. Syst. Biol.6 , 392 ( 2010 ).
  • Sivapalaratnam S , FarrugiaR , NieuwdorpMet al. Identification of candidate genes linking systemic inflammation to atherosclerosis; results of a human in vivo LPS infusion study . BMC Med. Genomic.10 , 4 – 64 ( 2011 ).
  • Matute JD , AriasAA , WrightNAet al. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40phox and selective defects I neutrophil NADPH oxidase activity . Blood114 , 3309 – 3315 ( 2009 ).
  • Fuhler GM , DrayerAL , VellengaE . Decreased phosphorylation of protein kinase B and extracellular signal-regulated kinase in neutrophils from patients with myelodysplasia . Blood101 , 1172 – 1180 ( 2003 ).
  • Muise AM , XuW , GuoCHet al. NADPH oxidase complex and IBD candidate gene studies: identification of a rare variant in NCF2 that results in reduced binding to RAC2 . Gut61 , 1028 – 1035 ( 2012 ).
  • Rak K , RaderDJ . The diet–microbe morbid union . Nature472 ( 7341 ), 40 – 41 ( 2011 ).
  • Lewis GD , WeiR , LiuEet al. Metabolite profiling of blood from individuals undergoing planned myocardial infarction reveals early markers of myocardial injury . J. Clin. Invest.118 , 3503 – 3512 ( 2008 ).
  • Meijers BK , Van KerckhovenS , VerbekeKet al. The uremic retention solute p-cresyl sulfate and markers of endothelial damage . Am. J. Kidney Dis.54 ( 5 ), 891 – 901 ( 2009 ).
  • Meijers BK , ClaesK , BammensBet al. p-Cresol and cardiovascular risk in mild-to-moderate kidney disease . Clin. J. Am. Soc. Nephrol.5 , 1182 – 1189 ( 2010 ).
  • Koppe L , PillonNJ , VellaREet al. p-Cresyl sulfate promotes insulin resistance associated with CKD . J. Am. Soc. Nephrol.24 ( 1 ), 88 – 99 ( 2013 ).
  • Yamamoto H , TsuruokaS , IokaTet al. Indoxyl sulfate stimulates proliferation of rat vascular smooth muscle cells . Kidney Int.69 , 1780 – 1785 ( 2006 ).
  • Dou L , Jourde-ChicheN , FaureVet al. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells . J. Thromb. Haemost.5 , 1302 – 1308 ( 2007 ).
  • Yu M , KimYJ , KangDH . Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress . Clin. J. Am. Soc. Nephrol.6 , 30 – 39 ( 2011 ).
  • Vaziri ND , YuanJ , NazertehraniS , NiZ , LiuS . Chronic kidney disease causes disruption of gastric and small intestinal epithelial tight junction . Am. J. Nephrol.38 ( 2 ), 99 – 103 ( 2013 ).
  • Vaziri ND , YuanJ , NorrisK . Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease . Am. J. Nephrol.37 ( 1 ), 1 – 6 ( 2013 ).
  • Vaziri ND , GoshtasbyN , YuanJet al. Uremic human plasma degrades intestinal epithelial barrier structure and function . Am. J. Nephrol.36 , 438 – 443 ( 2012 ).
  • Vaziri ND , YuanJ , KhazaeliM , MasudaY , IchiiH , LiuS . Oral activated charcoal adsorbent (AST-120) ameliorates CKD-induced intestinal epithelial barrier disruption and systemic inflammation . Am. J. Nephrol.37 , 518 – 525 ( 2013 ).
  • Liabeuf S , DrüekeTB , MassyZA . Protein-bound uremic toxins: new insight from clinical studies . Toxins3 , 911 – 919 ( 2011 ).
  • Meijers BKI , De PreterV , VerbekeKet al. p-Cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin . Nephrol. Dial. Transplant.25 , 219 – 224 ( 2010 ).
  • Meijers BK , EvenepoelP . The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression . Nephrol. Dial. Transplant.26 ( 3 ), 759 – 761 ( 2011 ).
  • Wu IW , HsuKH , LeeCCet al. p-Cresyl sulphate and indoxyl sulphate predict progression of chronic kidney disease . Nephrol. Dial. Transplant.26 ( 3 ), 938 – 947 ( 2011 ).
  • Hauser AB , StinghenAEM , GonçalvesSMet al. A gut feeling on endotoxemia: causes and consequences in chronic kidney disease . Nephron. Clin. Pract.118 , 165 – 172 ( 2011 ).
  • Terawaki H , YokoyamaK , YamadaYet al. Low-grade endotoxemia contributes to chronic inflammation in hemodialysis patients: examination with a novel lipopolysaccharide detection method . Ther. Apher. Dial.14 ( 5 ), 477 – 482 ( 2010 ).
  • Gollapudi P , YoonJ-W , GollapudiS , PahlMV , VaziriND . Effect of end stage renal disease and hemodialysis on expression and activities of leukocyte toll-like receptors (TLR) . Am. J. Nephrol.31 , 247 – 254 ( 2010 ).
  • Yoon JW , PahlMV , VaziriND . Spontaneous leukocyte activation and oxygen-free radical generation in end stage renal disease . Kidney Int.71 , 167 – 172 ( 2007 ).
  • Olsson J , JacobsonTA , PaulssonJMet al. Expression of neutrophil SOD2 is reduced after lipopolysaccharide stimulation: a potential cause of neutrophil dysfunction in chronic kidney disease . Nephrol. Dial. Transplant.26 ( 7 ), 2195 – 2201 ( 2011 ).
  • Shimazu S , HirashikiA , OkumuraTet al. Association between indoxyl sulfate and cardiac dysfunction and prognosis in patients with dilated cardiomyopathy . Circ. J.77 ( 2 ), 390 – 396 ( 2013 ).
  • Lin CJ , LiuHL , PanCFet al. Indoxyl sulfate predicts cardiovascular disease and renal function deterioration in advanced chronic kidney disease . Arch. Med. Res.43 ( 6 ), 451 – 456 ( 2012 ).
  • Bammens B , EvenepoelP , KeuleersHet al. Free serum concentrations of the protein-bound retention solute p-cresol predict mortality in hemodialysis patients . Kidney Int.69 , 1081 – 1087 ( 2006 ).
  • Liabeuf S , BarretoDV , BarretoFCet al. European uraemic toxin work group (EUTox): free p-cresylsulphate is a predictor of mortality in patients at different stages of chronic kidney disease . Nephrol. Dial. Transplant.25 ( 4 ), 1183 – 1191 ( 2010 ).
  • Winchester J , HostetterTH , MeyerTW . P-cresol sulfate: further understanding of its cardiovascular disease potential in CKD . Am. J. Kidney Dis.54 ( 5 ), 792 – 794 ( 2009 ).
  • Massy ZA , BarretoDV , BarretoFCet al. Uraemic toxins for consideration by the cardiologist-beyond traditional and non-traditional cardiovascular risk factors . Atherosclerosis211 , 381 – 383 ( 2010 ).
  • Bain MA , FaullR , FornasiniGet al. Accumulation of trimethylamine and trimethylamine-N-oxide in end-stage renal disease patients undergoing haemodialysis . Nephrol. Dial. Transplant.21 ( 5 ), 1300 – 1304 ( 2006 ).
  • Anders HJ , AndersenK , StecherB . The intestinal microbiota, a leaky gut, and abnormal immunity in kidney disease . Kidney Int.83 ( 6 ), 1010 – 1016 ( 2013 ).
  • Murthy M . Delineation of beneficial characteristics of effective probiotics . JAMA3 , 38 – 43 ( 2000 ).
  • O’Hara AM , ShanahanF . The gut flora as a forgotten organ . EMBO Rep.7 , 688 – 693 ( 2006 ).
  • Seth A , YanF , PolkDBet al. Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PCK and MAP kinase dependent mechanism . Am. J. Physiol. Gastrointest. Liver Physiol.294 , 1060 – 1069 ( 2008 ).
  • Ouwehand AC , TihonenK , SaarinenMet al. Influence of a combination of Lactobacillus acidophilus NCFM and lactitol on healthy elderly: intestinal and immune parameters . Br. J. Nutr.101 , 367 – 375 ( 2009 ).
  • Hegazy SK , El-BedewyMM . Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis . World J. Gastroenterol.16 ( 33 ), 4145 – 4151 ( 2010 ).
  • Oxman M , ShapiraR , KleinNet al. Oral administration of Lactobacillus induces cardioprotection . J. Altern. Complement. Med.7 ( 4 ), 345 – 354 ( 2001 ).
  • Simenhoff ML , DunnSR , ZollnerGPet al. Biomodulation of the toxic and nutritional effects of small bowel bacterial overgrowth in end-stage kidney disease using freeze-dried Lactobacillus acidophilus . Miner. Electrolyte Metab.22 ( 1–3 ), 92 – 96 ( 1996 ).
  • Takayama F , TakiK , NiwaT . Bifidobacterium in gastroresistant seamless capsule reduces serum levels of indoxyl sulfate in patients on hemodialysis . Am. J. Kidney Dis.41 , 142 – 145 ( 2003 ).
  • Taki K , TakayamamF , NiwaT . Beneficial effects of Bifidobacteria in a gastroresistant seamless capsule on hyperhomocysteinemia in hemodialysis patients . J. Ren. Nutr.15 , 77 – 80 ( 2005 ).
  • Ranganathan N , PatelB , RanganathanPet al. Probiotic amelioration of azotemia in 5/6th nephrectomized Sprague-Dawley rats . ScientificWorldJournal24 ( 5 ), 652 – 660 ( 2005 ).
  • Ranganathan N , RanganathanP , FriedmanEAet al. Pilot study of probiotic dietary supplementation for promoting healthy kidney function in patients with chronic kidney disease . Adv. Ther.27 ( 9 ), 634 – 647 ( 2010 ).
  • Broekaert WF , CourtinCM , VerbekeKet al. Prebiotic and other health-related effects of cereal-derived arabinoxylans, arabinoxylan-oligosaccharides, and xylooligosaccharides . Crit. Rev. Food Sci. Nutr.51 ( 2 ), 178 – 194(2011) .
  • Cloetens L , BroekaertWF , DelaedtYet al. Tolerance of arabinoxylan-oligosaccharides and their prebiotic activity in healthy subjects: a randomised, placebo-controlled cross-over study . Br. J. Nutr.103 ( 5 ), 703 – 713 ( 2010 ).
  • Nakabayashi I , NakamuraM , KawakamiKet al. Effects of synbiotic treatment on serum level of p-cresol in haemodialysis patients: a preliminary study . Nephrol. Dial. Transplant.26 ( 3 ), 1094 – 1098 ( 2011 ).
  • Ueda H , ShibaharaN , TakagiSet al. AST-120 treatment in pre-dialysis period affects the prognosis in patients on hemodialysis . Ren. Fail.30 , 856 – 860 ( 2008 ).
  • Vaziri ND , YuanJ , KhazaeliMet al. Oral activated charcoal adsorbent (AST-120) ameliorates chronic kidney disease-induced intestinal epithelial barrier disruption . Am. J. Nephrol.37 ( 6 ), 518 – 525 ( 2013 ).
  • Kruis W . Specific probiotics or ‘fecal transplantation’ . Dig. Dis.30 ( Suppl. 3 ), 81 – 84 ( 2012 ).
  • Vrieze A , de GrootPF , KootteRSet al. Fecal transplant: a safe and sustainable clinical therapy for restoring intestinal microbial balance in human disease? Best Pract Res Clin. Gastroenterol. 27 ( 1 ), 127 – 137 ( 2013 ).
  • Braat H , RottiersP , HommesDet al. A Phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease . Clin. Gastroenterol. Hepatol.4 , 754 – 769 ( 2006 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.