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BioMed Research International
Volume 2017 (2017), Article ID 5765417, 11 pages
https://doi.org/10.1155/2017/5765417
Review Article

Intestinal Barrier Disturbances in Haemodialysis Patients: Mechanisms, Consequences, and Therapeutic Options

1Department of Infection Immunity and Inflammation, College of Medicine, Biological Sciences and Psychology, University of Leicester, Leicester, UK
2John Walls Renal Unit, University Hospitals Leicester NHS Trust, Leicester, UK
3National Centre for Sport and Exercise Medicine and School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, UK
4Department of Cardiovascular Sciences, University of Leicester and NIHR Leicester Cardiovascular Biomedical Research Unit, Glenfield Hospital Leicester, Leicester, UK

Correspondence should be addressed to D. S. March; ku.ca.el@21msd

Received 31 October 2016; Accepted 20 December 2016; Published 17 January 2017

Academic Editor: Sabine Rohrmann

Copyright © 2017 D. S. March et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Kalantar-Zadeh, T. A. Ikizler, G. Block, M. M. Avram, and J. D. Kopple, “Malnutrition-inflammation complex syndrome in dialysis patients: causes and consequences,” American Journal of Kidney Diseases, vol. 42, no. 5, pp. 864–881, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. G. A. Kaysen, “Biochemistry and biomarkers of inflamed patients: why look, what to assess,” Clinical Journal of the American Society of Nephrology, vol. 4, no. 1, pp. S56–S63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Jofre, P. Rodriguez-Benitez, J. M. Lopez-Gomez, and R. Perez-Garcia, “Inflammatory Syndrome in Patients on Hemodialysis,” Journal of the American Society of Nephrology, vol. 17, no. 12, suppl 3, pp. S274–S280, 2006. View at Publisher · View at Google Scholar
  4. M. G. H. Betjes, “Immune cell dysfunction and inflammation in end-stage renal disease,” Nature Reviews Nephrology, vol. 9, no. 5, pp. 255–265, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Khoury, K. Tzukert, R. Abel, A. Abu Rmeileh, R. Levi, and Y. Ilan, “The gut-kidney axis in chronic renal failure: a new potential target for therapy,” Hemodialysis International, 2016. View at Publisher · View at Google Scholar
  6. N. D. Vaziri, Y.-Y. Zhao, and M. V. Pahl, “Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment,” Nephrology Dialysis Transplantation, vol. 31, no. 5, pp. 737–746, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Diebel, R. Kozol, R. F. Wilson, S. Mahajan, and D. Thomas, “Gastric intramucosal acidosis in patients with chronic kidney failure,” Surgery, vol. 5, no. 113, pp. 520–526, 1993. View at Google Scholar
  8. C. W. McIntyre, L. E. A. Harrison, M. T. Eldehni et al., “Circulating endotoxemia: a novel factor in systemic inflammation and cardiovascular disease in chronic kidney disease,” Clinical Journal of the American Society of Nephrology, vol. 6, no. 1, pp. 133–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. U. Feroze, K. Kalantar-Zadeh, K. A. Sterling et al., “Examining associations of circulating endotoxin with nutritional status, inflammation, and mortality in hemodialysis patients,” Journal of Renal Nutrition, vol. 22, no. 3, pp. 317–326, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Wang, H. Jiang, K. Shi, Y. Ren, P. Zhang, and S. Cheng, “Gut bacterial translocation is associated with microinflammation in end-stage renal disease patients,” Nephrology, vol. 17, no. 8, pp. 733–738, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. N. D. Vaziri, B. Dure‐Smith, R. Miller, and M. K. Mirahmadis, “Pathology of gastrointestinal tract in chronic hemodialysis patients: an autopsy study of 78 cases,” The American Journal of Gastroenterology, vol. 80, no. 8, pp. 608–611, 1985. View at Publisher · View at Google Scholar · View at Scopus
  12. U. Nisbeth, R. Hallgren, O. Eriksson, and B. G. Danielson, “Endotoxemia in chronic renal failure,” Nephron, vol. 45, no. 2, pp. 93–97, 1987. View at Google Scholar · View at Scopus
  13. T. Taniguchi, S. Katsushima, K. Lee et al., “Endotoxemia in patients on hemodialysis,” Nephron, vol. 56, no. 1, pp. 44–49, 1990. View at Google Scholar · View at Scopus
  14. C.-C. Szeto, B. C.-H. Kwan, K.-M. Chow et al., “Endotoxemia is related to systemic inflammation and atherosclerosis in peritoneal dialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 3, no. 2, pp. 431–436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. A. F. El-Koraie, Y. S. Naga, A. M. Saaran, N. G. Farahat, and W. A. Hazzah, “Endotoxins and inflammation in hemodialysis patients,” Hemodialysis International, vol. 17, no. 3, pp. 359–365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. B. C. Kwan, K. M. Chow, T. K. Ma et al., “Effect of using ultrapure dialysate for hemodialysis on the level of circulating bacterial fragment in renal failure patients,” Nephron Clinical Practice, vol. 123, no. 3-4, pp. 246–253, 2013. View at Publisher · View at Google Scholar
  17. K. R. Groschwitz and S. P. Hogan, “Intestinal barrier function: molecular regulation and disease pathogenesis,” Journal of Allergy and Clinical Immunology, vol. 124, no. 1, pp. 3–20, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. C. M. Van Itallie and J. M. Anderson, “Claudins and epithelial paracellular transport,” Annual Review of Physiology, vol. 68, pp. 403–429, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Crosnier, D. Stamataki, and J. Lewis, “Organizing cell renewal in the intestine: stem cells, signals and combinatorial control,” Nature Reviews Genetics, vol. 7, no. 5, pp. 349–359, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Grootjans, G. Thuijls, F. Verdam, J. P. Derikx, K. Lenaerts, and W. A. Buurman, “Non-invasive assessment of barrier integrity and function of the human gut,” World Journal of Gastrointestinal Surgery, vol. 2, no. 3, pp. 61–69, 2010. View at Google Scholar
  21. J. P. Derikx, M. D. Luyer, E. Heineman, and W. A. Buurman, “Non-invasive markers of gut wall integrity in health and disease,” World Journal of Gastroenterology, vol. 16, no. 42, pp. 5272–5279, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. L. González-Mariscal, R. Tapia, and D. Chamorro, “Crosstalk of tight junction components with signaling pathways,” Biochimica et Biophysica Acta—Biomembranes, vol. 1778, no. 3, pp. 729–756, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Shen, L. Su, and J. R. Turner, “Mechanisms and functional implications of intestinal barrier defects,” Digestive Diseases, vol. 27, no. 4, pp. 443–449, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. L. E. A. Harrison, J. O. Burton, C.-C. Szeto, P. K. T. Li, and C. W. McIntyre, “Endotoxaemia in haemodialysis: a novel factor in erythropoetin resistance?” PLoS ONE, vol. 7, no. 6, Article ID e40209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. S. G. John, P. J. Owen, L. E. A. Harrison et al., “The impact of antihypertensive drug therapy on endotoxemia in elderly patients with chronic kidney disease,” Clinical Journal of the American Society of Nephrology, vol. 6, no. 10, pp. 2389–2394, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. H. J. Jefferies, L. E. Crowley, L. E. A. Harrison et al., “Circulating endotoxaemia and frequent haemodialysis schedules,” Nephron Clinical Practice, vol. 128, no. 1-2, pp. 141–146, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. H. M. Markum, Suhardjono, H. T. Pohan, Suhendro, A. Lydia, and K. Inada, “Endotoxin in patients with terminal renal failure undergoing dialysis with re-processing dialyser,” Acta medica Indonesiana, vol. 36, no. 2, pp. 93–96, 2004. View at Google Scholar · View at Scopus
  28. J. F. Navarro-González, C. Mora-Fernández, M. Muros de Fuentes, J. Donate-Correa, V. Cazaña-Pérez, and J. García-Pérez, “Effect of phosphate binders on serum inflammatory profile, soluble CD14, and endotoxin levels in hemodialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 6, no. 9, pp. 2272–2279, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Raij, F. L. Shapiro, and A. F. Michael, “Endotoxemia in febrile reactions during hemodialysis,” Kidney International, vol. 4, no. 1, pp. 57–60, 1973. View at Publisher · View at Google Scholar · View at Scopus
  30. D. S. C. Raj, J. J. Carrero, V. O. Shah et al., “Soluble CD14 levels, interleukin 6, and mortality among prevalent hemodialysis patients,” American Journal of Kidney Diseases, vol. 54, no. 6, pp. 1072–1080, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. P. P. Sun, M. C. Perianayagam, and B. L. Jaber, “Endotoxin-binding affinity of sevelamer: a potential novel anti-inflammatory mechanism,” Kidney International. Supplement, no. 114, pp. S20–S25, 2009. View at Google Scholar · View at Scopus
  32. H. Suzuki, H. Honda, N. Kato et al., “Assessment of inflow of endotoxin and its fragments in patients on maintenance hemodialysis,” Blood Purification, vol. 31, no. 4, pp. 268–275, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Terawaki, K. Yokoyama, Y. Yamada et al., “Low-grade endotoxemia contributes to chronic inflammation in hemodialysis patients: examination with a novel lipopolysaccharide detection method,” Therapeutic Apheresis and Dialysis, vol. 14, no. 5, pp. 477–482, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. A. T. Bosenberg, J. G. Brock-Utne, S. L. Gaffin, M. T. B. Wells, and G. T. W. Blake, “Strenuous exercise causes systemic endotoxemia,” Journal of Applied Physiology, vol. 65, no. 1, pp. 106–108, 1988. View at Google Scholar · View at Scopus
  35. A. E. Jeukendrup, K. Vet-Joop, A. Sturk et al., “Relationship between gastro-intestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men,” Clinical Science, vol. 98, no. 1, pp. 47–55, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. K. L. Williams, Endotoxins: Pyrogens, LAL Testing and Depyrogenation, CRC Press, Boca Raton, Fla, USA, 2007.
  37. J. Wong, E. Vilar, and K. Farrington, “Endotoxemia in End-Stage Kidney Disease,” Seminars in Dialysis, vol. 28, no. 1, pp. 59–67, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. L. L. Chin and L. T. Mackinnon, “The roles of exercise-induced immune system disturbances in the pathology of heat stroke: the dual pathway model of heat stroke,” Sports Medicine, vol. 36, no. 1, pp. 39–64, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. U. Haglund, “Gut ischaemia,” Gut, vol. 35, no. 1, pp. S73–S76, 1994. View at Publisher · View at Google Scholar · View at Scopus
  40. J. C. Marshall, “The gut as a potential trigger of exercise-induced inflammatory responses,” Canadian Journal of Physiology and Pharmacology, vol. 76, no. 5, pp. 479–484, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Sakurada and J. R. S. Hales, “A role for gastrointestinal endotoxins in enhancement of heat tolerance by physical fitness,” Journal of Applied Physiology, vol. 84, no. 1, pp. 207–214, 1998. View at Google Scholar · View at Scopus
  42. P. Gathiram, S. L. Gaffin, J. G. Brock-Utne, and M. T. Wells, “Time course of endotoxemia and cardiovascular changes in heat-stressed primates,” Aviation, Space, and Environmental Medicine, vol. 58, no. 11, pp. 1071–1074, 1987. View at Google Scholar · View at Scopus
  43. A. B. Hauser, A. E. M. Stinghen, S. M. Gonçalves, S. Bucharles, and R. Pecoits-Filho, “A gut feeling on endotoxemia: causes and consequences in chronic kidney disease,” Nephron—Clinical Practice, vol. 118, no. 2, pp. c165–c172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. S. H. Lee, “Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases,” Intestinal Research, vol. 13, no. 1, pp. 11–18, 2015. View at Publisher · View at Google Scholar
  45. A. Nusrat, J. R. Turner, and J. L. Madara, “Molecular physiology and pathophysiology of tight junctions. IV. Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 279, no. 5, pp. G851–G857, 2000. View at Google Scholar · View at Scopus
  46. T. Eleftheriadis, V. Liakopoulos, K. Leivaditis, G. Antoniadi, and I. Stefanidis, “Infections in hemodialysis: a concise review—part 1: bacteremia and respiratory infections,” Hippokratia, vol. 15, no. 1, pp. 12–17, 2011. View at Google Scholar · View at Scopus
  47. G. Davison, “Bovine colostrum and immune function after exercise,” Medicine and Sport Science, vol. 59, pp. 62–69, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. C. J. Wiedermann, S. Kiechl, S. Dunzendorfer et al., “Association of endotoxemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck study,” Journal of the American College of Cardiology, vol. 34, no. 7, pp. 1975–1981, 1999. View at Publisher · View at Google Scholar · View at Scopus
  49. B. K. I. Meijers, H. De Loor, B. Bammens, K. Verbeke, Y. Vanrenterghem, and P. Evenepoel, “p-cresyl sulfate and indoxyl sulfate in hemodialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 4, no. 12, pp. 1932–1938, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. B. K. I. Meijers and P. Evenepoel, “The gut-kidney axis: indoxyl sulfate, p-cresyl sulfate and CKD progression,” Nephrology Dialysis Transplantation, vol. 26, no. 3, pp. 759–761, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Ramezani and D. S. Raj, “The gut microbiome, kidney disease, and targeted interventions,” Journal of the American Society of Nephrology, vol. 25, no. 4, pp. 657–670, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Schepers, G. Glorieux, and R. Vanholder, “The gut: the forgotten organ in Uremia?” Blood Purification, vol. 29, no. 2, pp. 130–136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. I.-W. Wu, K.-H. Hsu, C.-C. Lee et al., “P-cresyl sulphate and indoxyl sulphate predict progression of chronic kidney disease,” Nephrology Dialysis Transplantation, vol. 26, no. 3, pp. 938–947, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Bassilios, V. Menoyo, A. Berger et al., “Mesenteric ischaemia in haemodialysis patients: a case/control study,” Nephrology Dialysis Transplantation, vol. 18, no. 5, pp. 911–917, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. A. T. Blikslager, A. J. Moeser, J. L. Gookin, S. L. Jones, and J. Odle, “Restoration of barrier function in injured intestinal mucosa,” Physiological Reviews, vol. 87, no. 2, pp. 545–564, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Lindholm, H. Thysell, Y. Yamamoto, B. Forsberg, and C. A. Gullberg, “Temperature and vascular stability in hemodialysis,” Nephron, vol. 39, no. 2, pp. 130–133, 1985. View at Google Scholar · View at Scopus
  57. G. Davison, T. Marchbank, D. S. March, R. Thatcher, and R. J. Playford, “Zinc carnosine works with bovine colostrum in truncating heavy exercise-induced increase in gut permeability in healthy volunteers,” The American Journal of Clinical Nutrition, vol. 104, no. 2, pp. 526–536, 2016. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Dokladny, P. L. Moseley, and T. Y. Ma, “Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 290, no. 2, pp. G204–G212, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Marchbank, G. Davison, J. R. Oakes et al., “The nutriceutical bovine colostrum truncates the increase in gut permeability caused by heavy exercise in athletes,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 300, no. 3, pp. 477–484, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Gonçalves, R. Pecoits-Filho, S. Perreto et al., “Associations between renal function, volume status and endotoxaemia in chronic kidney disease patients,” Nephrology Dialysis Transplantation, vol. 21, no. 10, pp. 2788–2794, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Niebauer, H.-D. Volk, M. Kemp et al., “Endotoxin and immune activation in chronic heart failure: a prospective cohort study,” Lancet, vol. 353, no. 9167, pp. 1838–1842, 1999. View at Publisher · View at Google Scholar · View at Scopus
  62. N. M. Selby, J. O. Burton, L. J. Chesterton, and C. W. McIntyre, “Dialysis-induced regional left ventricular dysfunction is ameliorated by cooling the dialysate,” Clinical Journal of the American Society of Nephrology, vol. 1, no. 6, pp. 1216–1225, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Odudu, M. T. Eldehni, G. P. McCann, and C. W. McIntyre, “Randomized controlled trial of individualized dialysate cooling for cardiac protection in hemodialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 10, no. 8, pp. 1408–1417, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. M. T. Eldehni, A. Odudu, and C. W. McIntyre, “Randomized clinical trial of dialysate cooling and effects on brain white matter,” Journal of the American Society of Nephrology, vol. 26, no. 4, pp. 957–965, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. E. Segura-Ortí, “Exercise in hemodyalisis patients: a literature systematic review,” Nefrologia, vol. 30, no. 2, pp. 236–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Sheng, P. Zhang, L. Chen, J. Cheng, C. Wu, and J. Chen, “Intradialytic exercise in hemodialysis patients: a systematic review and meta-analysis,” American Journal of Nephrology, vol. 40, no. 5, pp. 478–490, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Dungey, N. C. Bishop, H. M. L. Young, J. O. Burton, and A. C. Smith, “The impact of exercising during haemodialysis on blood pressure, markers of cardiac injury and systemic inflammation—preliminary results of a pilot study,” Kidney and Blood Pressure Research, vol. 40, no. 6, pp. 593–604, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Konstantinidou, G. Koukouvou, E. Kouidi, A. Deligiannis, and A. Tourkantonis, “Exercise training in patients with end-stage renal disease on hemodialysis: comparison of three rehabilitation programs,” Journal of Rehabilitation Medicine, vol. 34, no. 1, pp. 40–45, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. E. Kouidi, D. Grekas, A. Deligiannis, and A. Tourkantonis, “Outcomes of long-term exercise training in dialysis patients: comparison of two training programs,” Clinical Nephrology, vol. 61, no. 1, pp. S31–S38, 2004. View at Google Scholar · View at Scopus
  70. J. G. Brock-Utne, S. L. Gaffin, M. T. Wells et al., “Endotoxaemia in exhausted runners after a long-distance race,” South African Medical Journal, vol. 73, no. 9, pp. 533–536, 1988. View at Google Scholar · View at Scopus
  71. G. Camus, J. Poortmans, M. Nys et al., “Mild endotoxaemia and the inflammatory response induced by a marathon race,” Clinical Science, vol. 92, no. 4, pp. 415–422, 1997. View at Publisher · View at Google Scholar · View at Scopus
  72. J. P. Clausen, “Effect of physical training on cardiovascular adjustments to exercise in man,” Physiological Reviews, vol. 57, no. 4, pp. 779–815, 1977. View at Google Scholar · View at Scopus
  73. L. B. Rowell, J. R. Blackmon, and R. A. Bruce, “Indocyanine green clearance and estimated hepatic blood flow during mild to maximal exercise in upright man,” The Journal of clinical investigation, vol. 43, pp. 1677–1690, 1964. View at Publisher · View at Google Scholar · View at Scopus
  74. K. L. Pals, R.-T. Chang, A. J. Ryan, and C. V. Gisolfi, “Effect of running intensity on intestinal permeability,” Journal of Applied Physiology, vol. 82, no. 2, pp. 571–576, 1997. View at Google Scholar · View at Scopus
  75. J. P. Cristol, B. Canaud, C. Mion, H. Rabesandratana, I. Gaillard, and A. Serre, “Enhancement of reactive oxygen species production and cell surface markers expression due to haemodialysis,” Nephrology Dialysis Transplantation, vol. 9, no. 4, pp. 389–394, 1994. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Descamps-Latscha, B. Goldfarb, A. T. Nguyen et al., “Establishing the relationship between complement activation and stimulation of phagocyte oxidative metabolism in hemodialyzed patients: a randomized prospective study,” Nephron, vol. 59, no. 2, pp. 279–285, 1991. View at Google Scholar · View at Scopus
  77. M. Dungey, N. C. Bishop, H. M. Young, J. O. Burton, and A. C. Smith, “SP565A Six-month intradialytic exercise programme has anti-inflammatory effects on circulating monocyte phenotypes and regulatory t cells but not on cytokine concentration,” Nephrology Dialysis Transplantation, vol. 30, supplement 3, p. iii565, 2015. View at Google Scholar
  78. J. Cros, N. Cagnard, K. Woollard et al., “Human CD14 dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors,” Immunity, vol. 33, no. 3, pp. 375–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. E. Shantsila, B. Wrigley, L. Tapp et al., “Immunophenotypic characterization of human monocyte subsets: possible implications for cardiovascular disease pathophysiology,” Journal of Thrombosis and Haemostasis, vol. 9, no. 5, pp. 1056–1066, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. G. H. Heine, C. Ulrich, E. Seibert et al., “CD14++CD16+ monocytes but not total monocyte numbers predict cardiovascular events in dialysis patients,” Kidney International, vol. 73, no. 5, pp. 622–629, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. F. S. Lira, J. C. Rosa, G. D. Pimentel et al., “Endotoxin levels correlate positively with a sedentary lifestyle and negatively with highly trained subjects,” Lipids in Health and Disease, vol. 9, article 82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. G. A. Selkirk, T. M. McLellan, H. E. Wright, and S. G. Rhind, “Mild endotoxemia, NF-κB translocation, and cytokine increase during exertional heat stress in trained and untrained individuals,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 295, no. 2, pp. R611–R623, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. P. L. Moseley, “Heat shock proteins and the inflammatory response,” Annals of the New York Academy of Sciences, vol. 856, pp. 206–213, 1998. View at Publisher · View at Google Scholar · View at Scopus
  84. S. M. Schneider and M. N. Zuhl, “HSP72 Up-regulation with heat acclimation,” Temperature, vol. 3, no. 1, pp. 28–30, 2016. View at Publisher · View at Google Scholar
  85. E. Fehrenbach, F. Passek, A. M. Niess et al., “HSP expression in human leukocytes is modulated by endurance exercise,” Medicine and Science in Sports and Exercise, vol. 32, no. 3, pp. 592–600, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. J. P. Morton, D. P. M. MacLaren, N. T. Cable et al., “Time course and differential responses of the major heat shock protein families in human skeletal muscle following acute nondamaging treadmill exercise,” Journal of Applied Physiology, vol. 101, no. 1, pp. 176–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Kuennen, T. Gillum, K. Dokladny, E. Bedrick, S. Schneider, and P. Moseley, “Thermotolerance and heat acclimation may share a common mechanism in humans,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 301, no. 2, pp. R524–R533, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. M. N. Zuhl, K. R. Lanphere, L. Kravitz et al., “Effects of oral glutamine supplementation on exercise-induced gastrointestinal permeability and tight junction protein expression,” Journal of Applied Physiology, vol. 116, no. 2, pp. 183–191, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. E. O. Petrof, K. Kojima, M. J. Ropeleski et al., “Probiotics inhibit nuclear factor-κB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition,” Gastroenterology, vol. 127, no. 5, pp. 1474–1487, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. J. D. Swales, J. D. Tange, and D. J. Evans, “Intestinal ammonia in uraemia: the effect of a urease inhibitor, acetohydroxamic acid,” Clinical Science, vol. 42, no. 1, pp. 105–112, 1972. View at Publisher · View at Google Scholar · View at Scopus
  91. N. D. Vaziri, N. Goshtasbi, J. Yuan et al., “Uremic plasma impairs barrier function and depletes the tight junction protein constituents of intestinal epithelium,” American Journal of Nephrology, vol. 36, no. 5, pp. 438–443, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. N. D. Vaziri, J. Yuan, and K. Norris, “Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease,” American Journal of Nephrology, vol. 37, no. 1, pp. 1–6, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Shi, F. Wang, H. Jiang et al., “Gut bacterial translocation may aggravate microinflammation in hemodialysis patients,” Digestive Diseases and Sciences, vol. 59, no. 9, pp. 2109–2117, 2014. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Ashida, M. Ogawa, M. Kim, H. Mimuro, and C. Sasakawa, “Bacteria and host interactions in the gut epithelial barrier,” Nature Chemical Biology, vol. 8, no. 1, pp. 36–45, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. W. L. Lau, K. Kalantar-Zadeh, and N. D. Vaziri, “The gut as a source of inflammation in chronic kidney disease,” Nephron, vol. 130, no. 2, pp. 92–98, 2015. View at Publisher · View at Google Scholar
  96. T. L. Sirich, N. S. Plummer, C. D. Gardner, T. H. Hostetter, and T. W. Meyer, “Effect of increasing dietary fiber on plasma levels of colon-derived solutes in hemodialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 9, no. 9, pp. 1603–1610, 2014. View at Publisher · View at Google Scholar · View at Scopus
  97. L.-M. Xie, Y.-Y. Ge, X. Huang, Y.-Q. Zhang, and J.-X. Li, “Effects of fermentable dietary fiber supplementation on oxidative and inflammatory status in hemodialysis patients,” International Journal of Clinical and Experimental Medicine, vol. 8, no. 1, pp. 1363–1369, 2015. View at Google Scholar · View at Scopus
  98. N. D. Vaziri, J. Yuan, M. Khazaeli, Y. Masuda, H. Ichii, and S. Liu, “Oral activated charcoal adsorbent (AST-120) ameliorates chronic kidney disease-induced intestinal epithelial barrier disruption,” American Journal of Nephrology, vol. 37, no. 6, pp. 518–525, 2013. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Akizawa, Y. Asano, S. Morita et al., “Effect of a carbonaceous oral adsorbent on the progression of CKD: a multicenter, randomized, controlled trial,” American Journal of Kidney Diseases, vol. 54, no. 3, pp. 459–467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. G. Schulman, T. Berl, G. J. Beck et al., “Randomized placebo-controlled EPPIC trials of AST-120 in CKD,” Journal of the American Society of Nephrology, vol. 26, no. 7, pp. 1732–1746, 2015. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Besarab, N. Amin, M. Ahsan et al., “Optimization of epoetin therapy with intravenous iron therapy in hemodialysis patients,” Journal of the American Society of Nephrology, vol. 11, no. 3, pp. 530–538, 2000. View at Google Scholar · View at Scopus
  102. S. H. Lee, P. Shinde, J. Choi et al., “Effects of dietary iron levels on growth performance, hematological status, liver mineral concentration, fecal microflora, and diarrhea incidence in weanling pigs,” Biological Trace Element Research, vol. 126, no. 1, pp. 57–68, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. G. R. Tompkins, N. L. O'Dell, I. T. Bryson, and C. B. Pennington, “The effects of dietary ferric iron and iron deprivation on the bacterial composition of the mouse intestine,” Current Microbiology, vol. 43, no. 1, pp. 38–42, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. M. B. Zimmermann, C. Chassard, F. Rohner et al., “The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire,” American Journal of Clinical Nutrition, vol. 92, no. 6, pp. 1406–1415, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Lee, T. Clavel, K. Smirnov et al., “Oral versus intravenous iron replacement therapy distinctly alters the gut microbiota and metabolome in patients with IBD,” Gut, 2015. View at Publisher · View at Google Scholar · View at Scopus
  106. A. S. Outschoorn, “Characterization of the USP reference standard endotoxin,” Progress in Clinical and Biological Research, vol. 93, pp. 115–119, 1982. View at Google Scholar · View at Scopus
  107. J. Cohen, “The detection and interpretation of endotoxaemia,” Intensive Care Medicine, Supplement, vol. 26, no. 1, pp. S51–S56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Kanda, K. Kubo, K. Hamasaki et al., “Influence of various hemodialysis membranes on the plasma (1→3)-β-D-glucan level,” Kidney International, vol. 60, no. 1, pp. 319–323, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Wong, Y. Zhang, A. Patidar et al., “Is endotoxemia in stable hemodialysis patients an artefact? Limitations of the limulus amebocyte lysate assay and role of (1→3)-β-D glucan,” PLOS ONE, vol. 11, no. 10, Article ID 0164978, 2016. View at Publisher · View at Google Scholar
  110. M. K. Dasgupta, “Biofilms and infection in dialysis patients,” Seminars in Dialysis, vol. 15, no. 5, pp. 338–346, 2002. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Bossola, M. Sanguinetti, D. Scribano et al., “Circulating bacterial-derived DNA fragments and markers of inflammation in chronic hemodialysis patients,” Clinical Journal of the American Society of Nephrology, vol. 4, no. 2, pp. 379–385, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. K. van Wijck, K. Lenaerts, L. J. C. van Loon, W. H. M. Peters, W. A. Buurman, and C. H. C. Dejong, “Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men,” PLoS ONE, vol. 6, no. 7, Article ID e22366, 2011. View at Publisher · View at Google Scholar · View at Scopus