The epithelium as a target in sepsis

Shock

Volumn 45, Issue 3, 2016, Pages 249-258

  Chawla, Lakhmir S ^a   Fink, Mitchell ^b   Goldstein, Stuart L ^c   Opal, Steven ^d   Gómez, Alonso ^e,f   Murray, Patrick ^g   Gómez, Hernando ^e,h   Kellum, John A ^h  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d BROWN UNIVERSITY   (United States)

^e Academia Colombiana de Medicina Critica (ACOMEC)   (Colombia)

^f Division of Critical Care Medicine   (Colombia)

^g UNIVERSITY COLLEGE DUBLIN   (Ireland)

^h UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Barrier function; epithelium; inflammation; sepsis; vectorial transport

Indexed keywords

BIOLOGICAL MARKER;

ADAPTATION; BLOOD PURIFICATION; EPITHELIUM; EPITHELIUM CELL; GLOMERULUS FILTRATION; HEMOFILTRATION; HUMAN; INTESTINE MUCOSA PERMEABILITY; KIDNEY DYSFUNCTION; KIDNEY PERFUSION; KIDNEY TUBULE; LIVER CELL; LUNG ALVEOLUS EPITHELIUM; LUNG FUNCTION; MICROBIOME; ORGAN INJURY; PURIFICATION; REVIEW; SEPSIS; SEPTIC SHOCK; SKIN DEFECT; TIDAL VOLUME; VENTILATOR INDUCED LUNG INJURY; ANIMAL; ANTIBODY SPECIFICITY; ION TRANSPORT; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; EPITHELIAL CELLS; EPITHELIUM; HUMANS; ION TRANSPORT; ORGAN SPECIFICITY; SEPSIS;

EID: 84959128932     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0000000000000518     Document Type: Review

References (98)

1. Structure, function, and diversity of the healthy human, microbiome. Nature 486: 207-214, 2012
2. Blaser MJ. The microbiome revolution. J Clin Investig 124: 4162-4165, 2014
3. Zeeuwen PL, Kleerebezem M, Timmerman HM, Schalkwijk J. Microbiome, and skin diseases. Curr Opin Allergy Clin Immunol 13: 514-520, 2013
4. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 9: 244-253, 2011
5. Martin DS, Goedhart P, Vercueil A, Ince C, Levett DZ, Grocott MP. Changes in sublingual microcirculatory flow index, and vessel density on ascent to altitude. Exp Physiol 95: 880-891, 2010
6. Boerma EC, Van Der Voort PH, Spronk PE, Ince C. Relationship between sublingual, and intestinal microcirculatory perfusion in patients with abdominal sepsis. Crit Care Med 35: 1055-1060, 2007
7. Gutierrez G, Ballarino G. Gutmucosal permeability, beta1 receptor blockers, and gastric tonometry: the time is now Intensive Care Med 37: 1721-1722, 2011
8. Gutierrez G, Brown SD. Gastric tonometry: a new monitoring modality in the intensive care unit. J Intensive Care Med 10: 34-44, 1995
9. Vadasz I, Raviv S, Sznajder JI. Alveolar epithelium, and Na, K-ATPase in acute lung injury. Intensive Care Med 33: 1243-1251, 2007
10. Walter JM, Wilson J, Ware LB. Biomarkers in acute respiratory distress syndrome: from pathobiology to improving patient care. Expert Rev Respir Med 8: 573-586, 2014
11. Ware LB, Koyama T, Zhao Z, Janz DR, Wickersham N, Bernard GR, et al. Biomarkers of lung epithelial injury, and inflammation distinguish severe sepsis patients with acute respiratory distress syndrome. Crit Care 17: R253, 2013
12. Terpstra ML, Aman J, Van Nieuw Amerongen GP, Groeneveld AB. Plasma biomarkers for acute respiratory distress syndrome: a systematic review, and meta-analysis. Crit Care Med 42: 691-700, 2014
13. Binnie A, Tsang JL, dos Santos CC. Biomarkers in acute respiratory distress syndrome. Curr Opin Crit Care 20: 47-55, 2014
14. Fink MP. Interpreting dual-sugar absorption studies in critically ill patients: what are the implications of apparent increases in intestinal permeability to hydrophilic solutes? Intensive Care Med 23: 489-492, 1997
15. Altshuler AE, Penn AH, Yang JA, Kim GR, Schmid-Schonbein GW. Protease activity increases in plasma, peritoneal fluid, and vital organs after hemorrhagic shock in rats. PLoS One 7: e32672, 2012
16. Chang M, Kistler EB, Schmid-SchonbeinGW: Disruption of the mucosal barrier during gut ischemia allows entry of digestive enzymes into the intestinal wall. Shock 37: 297-305, 2012
17. Penn AH, Schmid-Schonbein GW. The intestine as source of cytotoxic mediators in shock: free fatty acids, and degradation of lipid-binding proteins. Am J Physiol Heart Circ Physiol 294: H1779-H1792, 2008
18. Jorgensen VL, Nielsen SL, Espersen K, Perner A. Increased colorectal permeability in patients with severe sepsis, and septic shock. Intensive Care Med 32: 1790-1796, 2006
19. Doig CJ, Sutherland LR, Sandham JD, Fick GH, Verhoef M, Meddings JB. Increased intestinal permeability is associated with the development of multiple organ dysfunction syndrome in critically ill ICU patients. Am J Respir Crit Care Med 158: 444-451, 1998
20. Faries PL, Simon RJ, Martella AT, Lee MJ, Machiedo GW. Intestinal permeability correlates with severity of injury in trauma patients. J Trauma 44: 1031-1035, 1998
21. Kompan L, Kompan D. Importance of increased intestinal permeability after multiple injuries. Eur J Surg 167: 570-574, 2001
22. Besselink MG, Van Santvoort HC, Renooij W, de Smet MB, Boermeester MA, Fischer K, et al. Intestinal barrier dysfunction in a randomized trial of a specific probiotic composition in acute pancreatitis. Ann Surg 250: 712-719, 2009
23. Thuijls G, Derikx JP, de Haan JJ, Grootjans J, de Bruine A, Masclee AA, et al. Urine-based detection of intestinal tight junction loss. J Clin Gastroenterol 44: e14-e19, 2010
24. Derikx JP, Poeze M, Van Bijnen AA, Buurman WA, Heineman E. Evidence for intestinal, and liver epithelial cell injury in the early phase of sepsis. Shock 28: 544-548, 2007
25. Kosters A, Karpen SJ. The role of inflammation in cholestasis: clinical, and basic aspects. Semin Liver Dis 30: 186-194, 2010
26. Fan HB, Yang DL, Chen AS, Li Z, Xu LT, Ma XJ, et al. Sepsis-associated cholestasis in adult patients: a prospective study. Am J Med Sci 346: 462-466, 2013
27. Patel JJ, Taneja A, Niccum D, Kumar G, Jacobs E, Nanchal R. The association of serum bilirubin levels on the outcomes of severe sepsis. J Intensive Care Med 30(1): 23-29, 2015
28. Lora L, Mazzon E, Martines D, Fries W, Muraca M, Martin A, et al. Hepatocyte tight-junctional permeability is increased in rat experimental colitis. Gastroenterology 113: 1347-1354, 1997
29. Han X, Fink MP, Uchiyama T, Yang R, Delude RL. Increased iNOS activity is essential for hepatic epithelial tight junction dysfunction in endotoxemic mice. Am J Physiol Gastrointest Liver Physiol 286: G126-G136, 2004
30. Seymour CW, Yende S, Scott MJ, Pribis J, Mohney RP, Bell LN, et al. Metabolomics in pneumonia, and sepsis: an analysis of the GenIMS cohort study. Intensive Care Med 39: 1423-1434, 2013
31. Allen K, Jaeschke H, Copple BL. Bile acids induce inflammatory genes in hepatocytes: a novel mechanism of inflammation during obstructive cholestasis. Am J Pathol 178: 175-186, 2011
32. Hato T, Dagher PC. How the innate immune system senses trouble, and causes trouble. Clin J Am Soc Nephrol 10: 1459-1469, 2015
33. Takasu O, Gaut JP, Watanabe E, To K, Fagley RE, Sato B, et al. Mechanisms of cardiac, and renal dysfunction in patients dying of sepsis. Am J Respir Crit Care Med 187: 509-517, 2013
34. Vanmassenhove J, Glorieux G, Hoste E, Dhondt A, Vanholder R, Van BiesenW: Urinary output, and fractional excretion of sodium, and urea as indicators of transient versus intrinsic acute kidney injury during early sepsis. Crit Care 17: R234, 2013
35. Bagshaw SM, Bennett M, Devarajan P, Bellomo R. Urine biochemistry in septic, and non-septic acute kidney injury: a prospective observational study. J Crit Care 28: 371-378, 2013
36. Alge JL, Arthur JM. Biomarkers of AKI: a review of mechanistic relevance, and potential therapeutic implications. Clin J Am Soc Nephrol 10: 147-155, 2015
37. Chawla LS, Davison DL, Brasha-Mitchell E, Koyner JL, Arthur JM, Tumlin JA, et al. Development, and standardization of a furosemide stress test to predict the severity of acute kidney injury. Crit Care 17: R207, 2013
38. Koyner JL, Shaw AD, Chawla LS, Hoste EA, Bihorac A, Kashani K, Haase M, Shi J, Kellum JA; Sapphire Investigators: Tissue inhibitor metalloproteinase-2 (TIMP-2)IGF-binding protein-7 (IGFBP7) levels are associated with adverse long-term outcomes in patients withAKI. JAmSoc Nephrol 26: 1747-1754, 2015
39. Rimmelé T, Kellum JA. Clinical review: blood purification for sepsis. Crit Care 15: 205, 2011
40. Peng ZY, Bishop JV, Wen XY, et al. Modulation of chemokine gradients by apheresis redirects leukocyte trafficking to different compartments during sepsis, studies in a rat model. Crit Care 18: R141, 2014
41. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury, and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 342: 1301-1308, 2000
42. Amato MB, Barbas CS, Medeiros DM, Magaldi RB, Schettino GP, Lorenzi-Filho G, et al. Effect of a protective-ventilation strategy on mortality in the acute respiratory distress syndrome. N Engl J Med 338: 347-354, 1998
43. Villar J, Kacmarek RM, Perez-Mendez L, Aguirre-Jaime A. A high positive endexpiratory pressure, low tidal volume ventilatory strategy improves outcome in persistent acute respiratory distress syndrome: a randomized, controlled trial. Crit Care Med 34: 1311-1318, 2006
44. Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 157: 294-323, 1998
45. National Heart L, Blood Institute Acute Respiratory Distress Syndrome Clinical Trials N, Wiedemann HP, Wheeler AP, Bernard GR, Thompson BT, et al. Comparison of two fluid-management strategies in acute lung injury. N Engl J Med 354: 2564-2575, 2006
46. Fitzgerald M, Millar J, Blackwood B, Davies A, Brett SJ, McAuley DF, et al. Extracorporeal carbon dioxide removal for patients with acute respiratory failure secondary to the acute respiratory distress syndrome: a systematic review. Crit Care 18: 222, 2014
47. Cove ME, MacLaren G, Federspiel WJ, Kellum JA. Bench to bedside review: extracorporeal carbon dioxide removal, past present, and future. Crit Care 16: 232, 2012
48. Ding LA, Li JS. Effects of glutamine on intestinal permeability, and bacterial translocation in TPN-rats with endotoxemia. World J Gastroenterol 9: 1327-1332, 2003
49. Noth R, Hasler R, Stuber E, Ellrichmann M, Schafer H, Geismann C, et al. Oral glutamine supplementation improves intestinal permeability dysfunction in a murine acute graft-vs.-host disease model. Am J Physiol Gastrointest Liver Physiol 304: G646-G654, 2013
50. Mondello S, Galuppo M, Mazzon E, Domenico I, Mondello P, Carmela A, et al. Glutamine treatment attenuates the development of ischaemia/reperfusion injury of the gut. Eur J Pharmacol 643: 304-315, 2010
51. Kozar RA, Schultz SG, Bick RJ, Poindexter BJ, DeSoignie R, Moore FA. Enteral glutamine but not alanine maintains small bowel barrier function after ischemia/reperfusion injury in rats. Shock 21: 433-437, 2004
52. Peng X, Yan H, You Z, Wang P, Wang S. Effects of enteral supplementation with glutamine granules on intestinal mucosal barrier function in severe burned patients. Burns 30: 135-139, 2004
53. Van Der Hulst RR, Van Kreel BK, von Meyenfeldt MF, Brummer RJ, Arends JW, Deutz NE, et al. Glutamine, and the preservation of gut integrity. Lancet 341: 1363-1365, 1993
54. Zhou YP, Jiang ZM, Sun YH, Wang XR, Ma EL, Wilmore D. The effect of supplemental enteral glutamine on plasma levels, gut function, and outcome in severe burns: a randomized, double-blind, controlled clinical trial. JPEN J Parenter Enteral Nutr 27: 241-245, 2003
55. Luo M, Bazargan N, Griffith DP, Estivariz CF, Leader LM, Easley KA, et al. Metabolic effects of enteral versus parenteral alanyl-glutamine dipeptide administration in critically ill patients receiving enteral feeding: a pilot study. Clin Nutr 27: 297-306, 2008
56. Velasco N, Hernandez G, Wainstein C, Castillo L, Maiz A, Lopez F, et al. Influence of polymeric enteral nutrition supplemented with different doses of glutamine on gut permeability in critically ill patients. Nutrition 17: 907-911, 2001
57. Heyland D, Muscedere J, Wischmeyer PE, Cook D, Jones G, Albert M, et al. A randomized trial of glutamine, and antioxidants in critically ill patients. N Engl J Med 368: 1489-1497, 2013
58. Zhang JB, Du XG, Zhang H, Li ML, Xiao G, Wu J, et al. Breakdown of the gut barrier in patients with multiple organ dysfunction syndrome is attenuated by continuous blood purification: effects on tight junction structural proteins. Int J Artif Organs 33: 5-14, 2010
59. Shoji H. Extracorporeal endotoxin removal for the treatment of sepsis: endotoxin adsorption cartridge (Toraymyxin). Ther Apher Dial 7: 108-114, 2003
60. Rachoin JS, Foster D, Dellinger RP. Endotoxin removal: how far from the evidence? From EUPHAS to EUPHRATES. Contrib Nephrol 167: 111-118, 2010
61. Cruz DN, Perazella MA, Bellomo R, de Cal M, Polanco N, Corradi V, et al. Effectiveness of polymyxin B-immobilized fiber column in sepsis: a systematic review. Crit Care 11: R47, 2007
62. Lisboa LF, Asthana S, Kremer A, Swain M, Bagshaw SM, Gibney N, et al. Blood cytokine, chemokine, and gene expression in cholestasis patients with intractable pruritis treated with a molecular adsorbent recirculating system: a case series. Can J Gastroenterol 26: 799-805, 2012
63. Benyoub K, Muller M, Bonnet A, Simon R, Gazon M, Duperret S, et al. Amounts of bile acids, and bilirubin removed during single-pass albumin dialysis in patients with liver failure. Ther Apher Dial 15: 504-506, 2011
64. Stauber RE, Krisper P, Zollner G, Iberer F, Beuers U, Trauner M. Extracorporeal albumin dialysis in a patient with primary sclerosing cholangitis: effect on pruritus, and bile acid profile. Int J Artif Organs 27: 342-344, 2004
65. Boonsrirat U, Tiranathanagul K, Srisawat N, Susantitaphong P, Komolmit P, Praditpornsilpa K, Tungsanga K, Eiam-Ong S. Effective bilirubin reduction by single-pass albumin dialysis in liver failure. Artif Organs 33: 648-653, 2009
66. Lee KH, Wendon J, Lee M, Da Costa M, Lim SG, Tan KC. Predicting the decrease of conjugated bilirubin with extracorporeal albumin dialysis MARS using the predialysis molar ratio of conjugated bilirubin to albumin. Liver Transpl 8: 591-593, 2002
67. Chawla LS, Georgescu F, Abell B, Seneff MG, Kimmel PL. Modification of continuous venovenous hemodiafiltration with single-pass albumin dialysate allows for removal of serum bilirubin. Am J Kidney Dis 45: e51-e56, 2005
68. Kobashi-Margain RA, Gavilanes-Espinar JG, Gutierrez-Grobe Y, Gutierrez-Jimenez AA, Chavez-Tapia N, Ponciano-Rodriguez G, et al. Albumin dialysis with molecular adsorbent recirculating system (MARS) for the treatment of hepatic encephalopathy in liver failure. Ann Hepatol 10(Suppl 2): S70-S76, 2011
69. Jalan R, Williams R. Improvement in cerebral perfusion after MARS therapy: further clues about the pathogenesis of hepatic encephalopathy? Liver Transpl 7: 713-715, 2001
70. Goldstein SL, Chawla L, Ronco C, Kellum JA. Renal recovery. Crit Care 18: 301, 2014
71. Srisawat N, Wen X, Lee M, Kong L, Elder M, Carter M, et al. Urinary biomarkers, and renal recovery in critically ill patients with renal support. Clin J Am Soc Nephrol 6: 1815-1823, 2011
72. Cantaluppi V, Weber V, Lauritano C, Figliolini F, Beltramo S, Biancone L, et al. Protective effect of resin adsorption on septic plasma-induced tubular injury. Crit Care 14: R4, 2010
73. Peng ZY, Wang HZ, Carter MJ, Dileo MV, Bishop JV, Zhou FH, et al. Acute removal of common sepsis mediators does not explain the effects of extracorporeal blood purification in experimental sepsis. Kidney Int 81: 363-369, 2012
74. Lewis DA, Brown R, Williams J, White P, Jacobson SK, Marchesi JR, et al. The human urinary microbiome; bacterial DNA in voided urine of asymptomatic adults. Front Cell Infect Microbiol 3: 41, 2013
75. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age, and geography. Nature 486: 222-227, 2012
76. Sethi S. Molecular diagnosis of respiratory tract infection in acute exacerbations of chronic obstructive pulmonary disease. Clin Infect Dis 52(Suppl 4): S290-S295, 2011
77. Wedzicha JA. Role of viruses in exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 1: 115-120, 2004
78. Dickson RP, Erb-Downward JR, Huffnagle GB. The role of the bacterial microbiome in lung disease. Expert Rev Respir Med 7: 245-257, 2013
79. Huang YJ, Charlson ES, Collman RG, Colombini-Hatch S, Martinez FD, Senior RM. The role of the lung microbiome in health, and disease. A National Heart, Lung, and Blood Institute workshop report. Am J Respir Crit Care Med 187: 1382-1387, 2013
80. Kaiko GE, Stappenbeck TS. Host-microbe interactions shaping the gastrointestinal environment. Trends Immunol 35: 538-548, 2014
81. Human Microbiome Project C. Structure, function, and diversity of the healthy human microbiome. Nature 486: 207-214, 2012
82. Kolmeder CA, de Been M, Nikkila J, Ritamo I, Matto J, Valmu L, et al. Comparative metaproteomics, and diversity analysis of human intestinal microbiota testifies for its temporal stability, and expression of core functions. PLoS One 7: e29913, 2012
83. Babrowski T, Holbrook C, Moss J, Gottlieb L, Valuckaite V, Zaborin A, et al. Pseudomonas aeruginosa virulence expression is directly activated by morphine, and is capable of causing lethal gut-derived sepsis in mice during chronic morphine administration. Ann Surg 255: 386-393, 2012
84. Shimizu K, Ogura H, Hamasaki T, Goto M, Tasaki O, Asahara T, et al. Altered gut flora are associated with septic complications, and death in critically ill patients with systemic inflammatory response syndrome. Dig Dis Sci 56: 1171-1177, 2011
85. Wu L, Estrada O, Zaborina O, Bains M, Shen L, Kohler JE, et al. Recognition of host immune activation by Pseudomonas aeruginosa. Science 309: 774-777, 2005
86. Shimizu K, Ogura H, Asahara T, Nomoto K, Morotomi M, Tasaki O, et al. Probiotic/synbiotic therapy for treating critically ill patients from a gut microbiota perspective. Dig Dis Sci 58: 23-32, 2013
87. Barraud D, Bollaert PE, Gibot S. Impact of the administration of probiotics on mortality in critically ill adult patients: ameta-analysis of randomized controlled trials. Chest 143: 646-655, 2013
88. Trubiano JA, Gardiner B, Kwong JC, Ward P, Testro AG, Charles PG. Faecal microbiota transplantation for severe Clostridium difficile infection in the intensive care unit. Eur J Gastroenterol Hepatol 25: 255-257, 2013
89. Factor P, Dumasius V, Saldias F, Brown LA, Sznajder JI. Adenovirus-mediated transfer of an Na+/K+-ATPase beta1 subunit gene improves alveolar fluid clearance, and survival in hyperoxic rats. Hum Gene Ther 11: 2231-2242, 2000
90. Sugita M, Ferraro P, Dagenais A, Clermont ME, Barbry P, Michel RP, et al. Alveolar liquid clearance, and sodium channel expression are decreased in transplanted canine lungs. Am J Respir Crit Care Med 167: 1440-1450, 2003
91. Cher CD, Armugam A, Lachumanan R, Coghlan MW, Jeyaseelan K. Pulmonary inflammation, and edema induced by phospholipase A2: global gene analysis, and effects on aquaporins, and Na+/K+-ATPase. J Biol Chem 278: 31352-31360, 2003
92. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury, and the acute respiratory distress syndrome. Am J Respir Crit Care Med 163: 1376-1383, 2001
93. Schmidt C, Hocherl K, Schweda F, Bucher M. Proinflammatory cytokines cause down-regulation of renal chloride entry pathways during sepsis. Crit Care Med 35: 2110-2119, 2007
94. Carchman EH, Rao J, Loughran PA, Rosengart MR, Zuckerbraun BS. Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death, and hepatic injury from infection/sepsis in mice. Hepatology 53: 2053-2062, 2011
95. Hotchkiss RS, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, Matuschak GM, et al. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 27: 1230-1251, 1999
96. Pires-Neto RC, Morales MM, Lancas T, Inforsato N, Duarte MI, Amato MB, de Carvalho CR, da Silva LF, Mauad T, Dolhnikoff M. Expression of acute-phase cytokines, surfactant proteins, and epithelial apoptosis in small airways of human acute respiratory distress syndrome. J Crit Care 28(1): 111.e9-111.e15, 2013
97. Ranieri VM, Giunta F, Suter PM, Slutsky AS. Mechanical ventilation as a mediator of multisystem organ failure in acute respiratory distress syndrome. JAMA 284: 43-44, 2000
98. Imai Y, Parodo J, Kajikawa O, de Perrot M, Fischer S, Edwards V, et al. Injurious mechanical ventilation, and end-organ epithelial cell apoptosis, and organ dysfunction in an experimental model of acute respiratory distress syndrome. JAMA 289: 2104-2112, 2003