Biology of sepsis: Its relevance to pediatric nephrology

Pediatric Nephrology

Volumn 29, Issue 12, 2014, Pages 2273-2287

  Blatt, Neal B ^a   Srinivasan, Sushant ^b   Mottes, Theresa ^c   Shanley, Maureen M ^a   Shanley, Thomas P ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

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

Author keywords

Acute kidney injury; Host immune response; Intensive care; Multi organ dysfunction; Sepsis; Systemic inflammatory response syndrome

Indexed keywords

EID: 84891691789     PISSN: 0931041X     EISSN: 1432198X     Source Type: Journal    
DOI: 10.1007/s00467-013-2677-3     Document Type: Review

References (97)

1. Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ (1992) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. Chest 101:1644–1655
2. Goldstein B, Giroir B, Randolph A, International Consensus Conference on Pediatric Sepsis (2005) International pediatric sepsis consensus conference: definitions for sepsis and organ dysfunction in pediatrics. Pediatr Crit Care Med 6:2–8
3. Marshall JC (2000) Clinical trials of mediator-directed therapy in sepsis: what have we learned? Intensive Care Med 26(Suppl 1):S75–S83
4. Brierley J, Carcillo JA, Choong K, Cornell T, Decaen A, Deymann A, Doctor A, Davis A, Duff J, Dugas MA, Duncan A, Evans B, Feldman J, Felmet K, Fisher G, Frankel L, Jeffries H, Greenwald B, Gutierrez J, Hall M, Han YY, Hanson J, Hazelzet J, Hernan L, Kiff J, Kissoon N, Kon A, Irazuzta J, Lin J, Lorts A, Mariscalco M, Mehta R, Nadel S, Nguyen T, Nicholson C, Peters M, Okhuysen-Cawley R, Poulton T, Relves M, Rodriguez A, Rozenfeld R, Schnitzler E, Shanley T, Kache S, Skippen P, Torres A, von Dessauer B, Weingarten J, Yeh T, Zaritsky A, Stojadinovic B, Zimmerman J, Zuckerberg A (2009) Clinical practice parameters for hemodynamic support of pediatric and neonatal septic shock: 2007 update from the American College of Critical Care Medicine. Crit Care Med 37:666–688
5. El-Wiher N, Cornell TT, Kissoon N, Shanley TP (2011) Management and treatment guidelines for sepsis in pediatric patients. Open Inflamm J 4:101–109
6. Carcillo JA, Pollack MM, Ruttimann UE, Fields AI (1989) Sequential physiologic interactions in pediatric cardiogenic and septic shock. Crit Care Med 17:12–16
7. Ceneviva G, Paschall JA, Maffei F, Carcillo JA (1998) Hemodynamic support in fluid-refractory pediatric septic shock. Pediatrics 102:e19
8. Medzhitov R, Janeway C Jr (2000) The Toll receptor family and microbial recognition. Trends Microbiol 8:452–456
9. Kawai T, Akira S (2009) The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 21:317–337
10. Chan JK, Roth J, Oppenheim JJ, Tracey KJ, Vogl T, Feldmann M, Horwood N, Nanchahal J (2012) Alarmins: awaiting a clinical response. J Clin Invest 122:2711–2719
11. Denk S, Perl M, Huber-Lang M (2012) Damage- and pathogen-associated molecular patterns and alarmins: keys to sepsis? Eur Surg Res 48:171–179
12. Cerami A, Beutler B (1988) The role of cachectin/TNF in endotoxic shock and cachexia. Immunol Today 9:28–31
13. Schrier RW, Wang W (2004) Acute renal failure and sepsis. N Engl J Med 351:159–169
14. Ward PA, Gao H (2009) Sepsis, complement and the dysregulated inflammatory response. J Cell Mol Med 13:4154–4160
15. Cornell TT, Wynn J, Shanley TP, Wheeler DS, Wong HR (2010) Mechanisms and regulation of the gene-expression response to sepsis. Pediatrics 125:1248–1258
16. Oberholzer A, Oberholzer C, Moldawer LL (2002) Interleukin-10: a complex role in the pathogenesis of sepsis syndromes and its potential as an anti-inflammatory drug. Crit Care Med 30:S58–S63
17. Hotchkiss RS, Monneret G, Payen D (2013) Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 13:260–268
18. Wong HR, Cvijanovich N, Lin R, Allen GL, Thomas NJ, Willson DF, Freishtat RJ, Anas N, Meyer K, Checchia PA, Monaco M, Odom K, Shanley TP (2009) Identification of pediatric septic shock subclasses based on genome-wide expression profiling. BMC Med 7:34
19. Hall MW, Knatz NL, Vetterly C, Tomarello S, Wewers MD, Volk HD, Carcillo JA (2011) Immunoparalysis and nosocomial infection in children with multiple organ dysfunction syndrome. Intensive Care Med 37:525–532
20. Hotchkiss RS, Nicholson DW (2006) Apoptosis and caspases regulate death and inflammation in sepsis. Nat Rev Immunol 6:813–822
21. Torgersen C, Moser P, Luckner G, Mayr V, Jochberger S, Hasibeder WR, Dunser MW (2009) Macroscopic postmortem findings in 235 surgical intensive care patients with sepsis. Anesth Analg 108:1841–1847
22. Venet F, Lukaszewicz A-C, Payen D, Hotchkiss R, Monneret G (2013) Monitoring the immune response in sepsis: a rational approach to administration of immunoadjuvant therapies. Curr Opin Immunol 25:477–483
23. Mayeux PR, MacMillan-Crow LA (2012) Pharmacological targets in the renal peritubular microenvironment: implications for therapy for sepsis-induced acute kidney injury. Pharmacol Ther 134:139–155
24. Venkatachalam MA, Weinberg JM (2012) The tubule pathology of septic acute kidney injury: a neglected area of research comes of age. Kidney Int 81:338–340
25. Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL (2004) Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 32:1825–1831
26. Vincent JL, De Backer D (2005) Microvascular dysfunction as a cause of organ dysfunction in severe sepsis. Crit Care 9(Suppl 4):S9–S12
27. De Backer D, Donadello K, Sakr Y, Ospina-Tascon G, Salgado D, Scolletta S, Vincent JL (2013) Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med 41:791–799
28. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ (2004) Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 172:2629–2635
29. Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA, Quigg RJ (2002) Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol 168:5817–5823
30. Pathak E, MacMillan-Crow LA, Mayeux PR (2012) Role of mitochondrial oxidants in an in vitro model of sepsis-induced renal injury. J Pharmacol Exp Ther 340:192–201
31. Lee SY, Lee YS, Choi HM, Ko YS, Lee HY, Jo SK, Cho WY, Kim HK (2012) Distinct pathophysiologic mechanisms of septic acute kidney injury: role of immune suppression and renal tubular cell apoptosis in murine model of septic acute kidney injury. Crit Care Med 40:2997–3006
32. Wang Z, Holthoff JH, Seely KA, Pathak E, Spencer HJ 3rd, Gokden N, Mayeux PR (2012) Development of oxidative stress in the peritubular capillary microenvironment mediates sepsis-induced renal microcirculatory failure and acute kidney injury. Am J Pathol 180:505–516
33. Holthoff JH, Wang Z, Seely KA, Gokden N, Mayeux PR (2012) Resveratrol improves renal microcirculation, protects the tubular epithelium, and prolongs survival in a mouse model of sepsis-induced acute kidney injury. Kidney Int 81:370–378
34. Wu L, Tiwari MM, Messer KJ, Holthoff JH, Gokden N, Brock RW, Mayeux PR (2007) Peritubular capillary dysfunction and renal tubular epithelial cell stress following lipopolysaccharide administration in mice. Am J Physiol Renal Physiol 292:F261–F268
35. Benes J, Chvojka J, Sykora R, Radej J, Krouzecky A, Novak I, Matejovic M (2011) Searching for mechanisms that matter in early septic acute kidney injury: an experimental study. Crit Care 15:R256
36. Langenberg C, Wan L, Egi M, May CN, Bellomo R (2006) Renal blood flow in experimental septic acute renal failure. Kidney Int 69:1996–2002
37. Wolfs TG, Buurman WA, van Schadewijk A, de Vries B, Daemen MA, Hiemstra PS, van’t Veer C (2002) In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-gamma and TNF-alpha mediated up-regulation during inflammation. J Immunol 168:1286–1293
38. Goncalves GM, Zamboni DS, Camara NO (2010) The role of innate immunity in septic acute kidney injuries. Shock 34(Suppl 1):22–26
39. Bonegio R, Lieberthal W (2002) Role of apoptosis in the pathogenesis of acute renal failure. Curr Opin Nephrol Hypertens 11:301–308
40. Jo SK, Cha DR, Cho WY, Kim HK, Chang KH, Yun SY, Won NH (2002) Inflammatory cytokines and lipopolysaccharide induce Fas-mediated apoptosis in renal tubular cells. Nephron 91:406–415
41. Gando S (2010) Microvascular thrombosis and multiple organ dysfunction syndrome. Crit Care Med 38:S35–S42
42. Hook KM, Abrams CS (2012) The loss of homeostasis in hemostasis: new approaches in treating and understanding acute disseminated intravascular coagulation in critically ill patients. Clin Transl Sci 5:85–92
43. Nguyen TC, Carcillo JA (2006) Bench-to-bedside review: thrombocytopenia-associated multiple organ failure–a newly appreciated syndrome in the critically ill. Crit Care 10:235
44. Nguyen T, Hall M, Han Y, Fiedor M, Hasset A, Lopez-Plaza I, Watson S, Lum L, Carcillo JA (2001) Microvascular thrombosis in pediatric multiple organ failure: Is it a therapeutic target? Pediatr Crit Care Med 2:187–196
45. Claus RA, Bockmeyer CL, Sossdorf M, Losche W (2010) The balance between von-Willebrand factor and its cleaving protease ADAMTS13: biomarker in systemic inflammation and development of organ failure? Curr Mol Med 10:236–248
46. Bellomo R, Ronco C, Kellum JA, Mehta RL, Palevsky P, Acute Dialysis Quality Initiative workgroup (2004) Acute renal failure - definition, outcome measures, animal models, fluid therapy and information technology needs: the Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit Care 8:R204–R212
47. Akcan-Arikan A, Zappitelli M, Loftis LL, Washburn KK, Jefferson LS, Goldstein SL (2007) Modified RIFLE criteria in critically ill children with acute kidney injury. Kidney Int 71:1028–1035
48. Mehta R, Kellum J, Shah S, Molitoris B, Ronco C, Warnock D, Levin A (2007) Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care 11:R31
49. KDIGO (2012) Clinical practice guideline for acute kidney injury. Section 2: AKI definition. Kidney Int Suppl 2:19–36
50. Vachvanichsanong P, Dissaneewate P, Lim A, McNeil E (2006) Childhood acute renal failure: 22-year experience in a university hospital in southern Thailand. Pediatrics 118:e786–e791
51. Pundziene B, Dobiliene D, Rudaitis S (2010) Acute kidney injury in pediatric patients: experience of a single center during an 11-year period. Medicina (Kaunas) 46:511–515
52. Plotz FB, Hulst HE, Twisk JW, Bokenkamp A, Markhorst DG, van Wijk JA (2005) Effect of acute renal failure on outcome in children with severe septic shock. Pediatr Nephrol 20:1177–1181
53. Ghani AA, Al Helal B, Hussain N (2009) Acute renal failure in pediatric patients: etiology and predictors of outcome. Saudi J Kidney Dis Transpl 20:69–76
54. Hui-Stickle S, Brewer ED, Goldstein SL (2005) Pediatric ARF epidemiology at a tertiary care center from 1999 to 2001. Am J Kidney Dis 45:96–101
55. Miller ME, Williams JA (2002) Chronic renal failure in Jamaican children. West Indian Med J 51:220–224
56. Bailey D, Phan V, Litalien C, Ducruet T, Merouani A, Lacroix J, Gauvin F (2007) Risk factors of acute renal failure in critically ill children: a prospective descriptive epidemiological study. Pediatr Crit Care Med 8:29–35
57. Plotz FB, Bouma AB, van Wijk JA, Kneyber MC, Bokenkamp A (2008) Pediatric acute kidney injury in the ICU: an independent evaluation of pRIFLE criteria. Intensive Care Med 34:1713–1717
58. Palmieri T, Lavrentieva A, Greenhalgh D (2009) An assessment of acute kidney injury with modified RIFLE criteria in pediatric patients with severe burns. Intensive Care Med 35:2125–2129
59. Duzova A, Bakkaloglu A, Kalyoncu M, Poyrazoglu H, Delibas A, Ozkaya O, Peru H, Alpay H, Soylemezoglu O, Gur-Guven A, Bak M, Bircan Z, Cengiz N, Akil I, Ozcakar B, Uncu N, Karabay-Bayazit A, Sonmez F (2010) Turkish Society for Pediatric Nephrology Acute Kidney Injury Study Group. Etiology and outcome of acute kidney injury in children. Pediatr Nephrol 25:1453–1461
60. Goldstein SL, Chawla LS (2010) Renal angina. Clin J Am Soc Nephrol 5:943–949
61. Basu RK, Chawla LS, Wheeler DS, Goldstein SL (2012) Renal angina: an emerging paradigm to identify children at risk for acute kidney injury. Pediatr Nephrol 27:1067–1078
62. Basu RK, Zappitelli M, Brunner L, Wang Y, Wong HR, Chawla LS, Wheeler DS, Goldstein SL (2013) Derivation and validation of the renal angina index to improve the prediction of acute kidney injury in critically ill children. Kidney Int. doi:10.1038/ki.2013.349
63. Mehta RL, Bouchard J, Soroko SB, Ikizler TA, Paganini EP, Chertow GM, Himmelfarb J, Program to Improve Care in Acute Renal Disease Study Group (2011) Sepsis as a cause and consequence of acute kidney injury: Program to Improve Care in Acute Renal Disease. Intensive Care Med 37:241–248
64. Levy EM, Viscoli CM, Horwitz RI (1996) The effect of acute renal failure on mortality. A cohort analysis. JAMA 275:1489–1494
65. de Jager DJ, Grootendorst DC, Jager KJ, van Dijk PC, Tomas LMJ, Ansell D, Collart F, Finne P, Heaf JG, Meester JD, Wetzels JFM, Rosendaal FR, Dekker FW (2009) Cardiovascular and noncardiovascular mortality among patients starting dialysis. JAMA 302:1782–1789
66. Eleftheriadis T, Antoniadi G, Liakopoulos V, Kartsios C, Stefanidis I (2007) Disturbances of acquired immunity in hemodialysis patients. Semin Dial 20:440–451
67. Wong HR, Cvijanovich N, Allen GL, Lin R, Anas N, Meyer K, Freishtat RJ, Monaco M, Odoms K, Sakthivel B, Shanley TP (2009) Genomics of Pediatric SIRS/Septic Shock Investigators. Genomic expression profiling across the pediatric systemic inflammatory response syndrome, sepsis, and septic shock spectrum. Crit Care Med 37:1558–1566
68. Girndt M, Sester M, Sester U, Kaul H, Kohler H (2001) Molecular aspects of T- and B-cell function in uremia. Kidney Int 59(Suppl 78):S206–S211
69. Chonchol M (2006) Neutrophil dysfunction and infection risk in end-stage renal disease. Semin Dial 19:291–296
70. Sardenberg C, Suassuna P, Andreoli MCC, Watanabe R, Dalboni MA, Manfredi SR, dos Santos OP, Kallas e.g., Draibe SA, Cendoroglo M (2006) Effects of uraemia and dialysis modality on polymorphonuclear cell apoptosis and function. Nephrol Dial Transplant 21:160–165
71. Carracedo J, Ramirez R, Soriano S, Alvarez de Lara MA, Rodriguez M, Martin-Malo A, Aljama P (2005) Monocytes from dialysis patients exhibit characteristics of sensescent cells: does it really mean inflammation? Contrib Nephrol 149:208–218
72. Himmelfarb J (2009) Uremic toxicity, oxidative stress, and hemodialysis as renal replacement therapy. Semin Dial 22:636–643
73. Daichou Y, Kurashige S, Hasimoto S, Suzuki S (1999) Characteristic cytokine products of Th1 and Th2 cells in hemodialysis patients. Nephron 83:237–245
74. Meier P, Dayer E, Blanc E, Wauters J-P (2002) Early T cell activation correlates with expression of apoptosis markers in patients with end-stage renal disease. J Am Soc Nephrol 13:204–212
75. Czaja AS, Zummerman JJ, Nathens AB (2009) Readmission and late mortality after pediatric severe sepsis. Pediatrics 123:849–857
76. Alvarez-Lara MA, Carracedo J, Ramirez R, Martin-Malo A, Rodriguez M, Madueño JA, Alijama P (2004) The imbalance in the ratio of Th1 and Th2 helper lymphocytes in uraemia is mediated by an increased apoptosis of Th1 subset. Nephrol Dial Transplant 19:3084–3090
77. Labriola L, Crott R, Jadoul M (2008) Preventing haemodialysis catheter-related bacteraemia with an antimicrobial lock solution: a meta-analysis of prospective randomized trials. Nephrol Dial Transplant 23:1666–1672
78. Stefanidis CJ (2009) Prevention of catheter-related bacteremia in children on hemodialysis: time for action. Pediatr Nephrol 24:2087–2095
79. KDIGO (2012) Clinical practice guideline for acute kidney injury. Chapter 5.4: Vascular access for renal replacement therapy in AKI. Kidney Int Suppl 2:101–104
80. Sutton TA (2009) Alteration of microvascular permeability in acute kidney injury. Microvasc Res 77:4–7
81. Foland JA, Fortenberry JD, Warshaw BL, Pettignano R, Merritt RK, Heard ML, Rogers K, Reid C, Tanner AJ, Easley KA (2004) Fluid overload before continuous hemofiltration and survival in critically ill children: a retrospective analysis. Crit Care Med 32:1771–1776
82. Selewski DT, Cornell TT, Blatt NB, Han YY, Mottes T, Kommareddi M, Gaies MG, Annich GM, Kershaw DB, Shanley TP, Heung M (2012) Fluid overload and fluid removal in pediatric patients on extracorporeal membrane oxygenation requiring continuous renal replacement therapy. Crit Care Med 40:2694–2699
83. Goldstein SL (2009) Overview of pediatric renal replacement therapy in acute kidney injury. Semin Dial 22:180–184
84. Maclaren G, Butt W (2009) Controversies in paediatric continuous renal replacement therapy. Intensive Care Med 35:596–602
85. Ronco C, Tetta C, Mariano F, Wratten ML, Bonello M, Bordoni V, Cardona X, Inguaggiato P, Pilotto L, d’Intini V, Bellomo R (2003) Interpreting the mechanisms of continuous renal replacement therapy in sepsis: the peak concentration hypothesis. Artif Organs 27:792–801
86. John S, Eckardt KU (2007) Renal replacement strategies in the ICU. Chest 132:1379–1388
87. Ronco C, Bellomo R, Homel P, Brendolan A, Dan M, Piccinni P, La Greca G (2000) Effects of different doses in continuous veno-venous haemofiltration on outcomes of acute renal failure: a prospective randomised trial. Lancet 356:26–30
88. Saudan P, Niederberger M, De Seigneux S, Romand J, Pugin J, Perneger T, Martin PY (2006) Adding a dialysis dose to continuous hemofiltration increases survival in patients with acute renal failure. Kidney Int 70:1312–1317
89. Tolwani AJ, Campbell RC, Stofan BS, Lai KR, Oster RA, Wille KM (2008) Standard versus high-dose CVVHDF for ICU-related acute renal failure. J Am Soc Nephrol 19:1233–1238
90. VA/NIH Acute Renal Failure Trial Network, Palevsky PM, Zhang JH, O’Connor TZ, Chertow GM, Crowley ST, Choudhury D, Finkel K, Kellum JA, Paganini E, Schein RM, Smith MW, Swanson KM, Thompson BT, Vijayan A, Watnick S, Star RA, Peduzzi P (2008) Intensity of renal support in critically ill patients with acute kidney injury. N Engl J Med 359:7–20
91. Ghani RA, Zainudin S, Ctkong N, Rahman AF, Wafa SR, Mohamad M, Manaf MR, Ismail R (2006) Serum IL-6 and IL-1-ra with sequential organ failure assessment scores in septic patients receiving high-volume haemofiltration and continuous venovenous haemofiltration. Nephrology (Carlton) 11:386–393
92. Morgera S, Haase M, Kuss T, Vargas-Hein O, Zuckermann-Becker H, Melzer C, Krieg H, Wegner B, Bellomo R, Neumayer HH (2006) Pilot study on the effects of high cutoff hemofiltration on the need for norepinephrine in septic patients with acute renal failure. Crit Care Med 34:2099–2104
93. Morgera S, Slowinski T, Melzer C, Sobottke V, Vargas-Hein O, Volk T, Zuckermann-Becker H, Wegner B, Muller JM, Baumann G, Kox WJ, Bellomo R, Neumayer HH (2004) Renal replacement therapy with high-cutoff hemofilters: impact of convection and diffusion on cytokine clearances and protein status. Am J Kidney Dis 43:444–453
94. De Vriese AS, Colardyn FA, Philippe JJ, Vanholder RC, De Sutter JH, Lameire NH (1999) Cytokine removal during continuous hemofiltration in septic patients. J Am Soc Nephrol 10:846–853
95. Haase M, Silvester W, Uchino S, Goldsmith D, Davenport P, Tipping P, Boyce N, Bellomo R (2007) A pilot study of high-adsorption hemofiltration in human septic shock. Int J Artif Organs 30:108–117
96. Hirasawa H, Oda S, Nakamura M, Watanabe E, Shiga H, Matsuda K (2012) Continuous hemodiafiltration with a cytokine-adsorbing hemofilter for sepsis. Blood Purif 34:164–170
97. Zarjou A, Agarwal A (2011) Sepsis and acute kidney injury. J Am Soc Nephrol 22:999–1006