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Clinical and Experimental Nephrology
Published in: Clinical and Experimental Nephrology 4/2011

01-08-2011 | Review Article

Lung injury following acute kidney injury: kidney–lung crosstalk

Authors: Kent Doi, Tomoko Ishizu, Toshiro Fujita, Eisei Noiri

Published in: Clinical and Experimental Nephrology | Issue 4/2011

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Abstract

The mortality of acute kidney injury (AKI) remains unacceptably high, especially associated with acute respiratory failure. Lung injury complicated with AKI was previously considered as “uremic lung”, which is characterized by volume overload and increased vascular permeability. New experimental data using rodent models of renal ischemia–reperfusion and bilateral nephrectomy have emerged recently focusing on kidney–lung crosstalk in AKI, and have highlighted the pathophysiological significance of increased cytokine concentration, enhanced inflammatory responses, and neutrophil activation. In this review, we outline the history of uremic lung and acute lung injury (ALI)/acute respiratory distress syndrome (ARDS), the epidemiological data on the synergistic effect of AKI and lung injury on mortality, and recent basic research which has identified possible pathways in AKI-induced lung injury. These findings will enable us to develop new therapeutic strategies against lung injury associated with AKI and improve the outcomes of critically ill patients in intensive care units.
Literature
1.
Chertow GM, Christiansen CL, Cleary PD, Munro C, Lazarus JM. Prognostic stratification in critically ill patients with acute renal failure requiring dialysis. Arch Intern Med. 1995;155:1505–11.CrossRefPubMed
2.
Chertow GM, Lazarus JM, Paganini EP, Allgren RL, Lafayette RA, Sayegh MH. Predictors of mortality and the provision of dialysis in patients with acute tubular necrosis. The Auriculin Anaritide Acute Renal Failure Study Group. J Am Soc Nephrol. 1998;9:692–8.PubMed
3.
Metnitz PG, Krenn CG, Steltzer H, Lang T, Ploder J, Lenz K, et al. Effect of acute renal failure requiring renal replacement therapy on outcome in critically ill patients. Crit Care Med. 2002;30:2051–8.CrossRefPubMed
4.
Mehta RL, Pascual MT, Gruta CG, Zhuang S, Chertow GM. Refining predictive models in critically ill patients with acute renal failure. J Am Soc Nephrol. 2002;13:1350–7.CrossRefPubMed
5.
Scheel PJ, Liu M, Rabb H. Uremic lung: new insights into a forgotten condition. Kidney Int. 2008;74:849–51.CrossRefPubMed
6.
Kelly KJ. Distant effects of experimental renal ischemia/reperfusion injury. J Am Soc Nephrol. 2003;14:1549–58.CrossRefPubMed
7.
Liu M, Liang Y, Chigurupati S, Lathia JD, Pletnikov M, Sun Z, et al. Acute kidney injury leads to inflammation and functional changes in the brain. J Am Soc Nephrol. 2008;19:1360–70.CrossRefPubMedPubMedCentral
8.
Liu KD, Matthay MA. Advances in critical care for the nephrologist: acute lung injury/ARDS. Clin J Am Soc Nephrol. 2008;3:578–86.CrossRefPubMed
9.
Lange W. Uber eine eigentumliche Erkrankung der kleinen Bronchien obliterans. Dtsch Arch Klin Med. 1901;70:342–64.
10.
Roubier CH, Plauchu M. Sur certain aspects radiographiques de l’oedeme pulmonaire chez les cardio-renaux. Lyon méd. 1933;152:137.
11.
12.
Rackow EC, Fein IA. Fulminant noncardiogenic pulmonary edema in the critically ill. Crit Care Med. 1978;6:360–3.CrossRefPubMed
13.
Bleyl U, Sander E, Schindler T. The pathology and biology of uremic pneumonitis. Intensive Care Med. 1981;7:193–202.CrossRefPubMed
14.
15.
Faubel S. Pulmonary complications after acute kidney injury. Adv Chronic Kidney Dis. 2008;15:284–96.CrossRefPubMed
16.
Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet. 1967;2:319–23.CrossRefPubMed
17.
Oud L. From DaNang lung to combat trauma-associated acute lung injury-closing the loop. South Med J. 2009;102:567–8.CrossRefPubMed
18.
Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, et al. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med. 1994;149:818–24.CrossRefPubMed
19.
20.
Ware LB. Pathophysiology of acute lung injury and the acute respiratory distress syndrome. Semin Respir Crit Care Med. 2006;27:337–49.CrossRefPubMed
21.
Russell JA, Singer J, Bernard GR, Wheeler A, Fulkerson W, Hudson L, et al. Changing pattern of organ dysfunction in early human sepsis is related to mortality. Crit Care Med. 2000;28:3405–11.CrossRefPubMed
22.
Mehta RL, Pascual MT, Soroko S, Savage BR, Himmelfarb J, Ikizler TA, et al. Spectrum of acute renal failure in the intensive care unit: the PICARD experience. Kidney Int. 2004;66:1613–21.CrossRefPubMed
23.
Liu KD, Glidden DV, Eisner MD, Parsons PE, Ware LB, Wheeler A, et al. Predictive and pathogenetic value of plasma biomarkers for acute kidney injury in patients with acute lung injury. Crit Care Med. 2007;35:2755–61.PubMedPubMedCentral
24.
Vieira JM Jr, Castro I, Curvello-Neto A, Demarzo S, Caruso P, Pastore L Jr, et al. Effect of acute kidney injury on weaning from mechanical ventilation in critically ill patients. Crit Care Med. 2007;35:184–91.CrossRefPubMed
25.
Feltes CM, Van Eyk J, Rabb H. Distant-organ changes after acute kidney injury. Nephron Physiol. 2008;109:p80–4.CrossRefPubMed
26.
27.
Rabb H, Wang Z, Nemoto T, Hotchkiss J, Yokota N, Soleimani M. Acute renal failure leads to dysregulation of lung salt and water channels. Kidney Int. 2003;63:600–6.CrossRefPubMed
28.
Kramer AA, Postler G, Salhab KF, Mendez C, Carey LC, Rabb H. Renal ischemia/reperfusion leads to macrophage-mediated increase in pulmonary vascular permeability. Kidney Int. 1999;55:2362–7.CrossRefPubMed
29.
Deng J, Hu X, Yuen PS, Star RA. Alpha-melanocyte-stimulating hormone inhibits lung injury after renal ischemia/reperfusion. Am J Respir Crit Care Med. 2004;169:749–56.CrossRefPubMed
30.
Star RA, Rajora N, Huang J, Stock RC, Catania A, Lipton JM. Evidence of autocrine modulation of macrophage nitric oxide synthase by alpha-melanocyte-stimulating hormone. Proc Natl Acad Sci USA. 1995;92:8016–20.CrossRefPubMed
31.
Kohda Y, Chiao H, Star RA. Alpha-melanocyte-stimulating hormone and acute renal failure. Curr Opin Nephrol Hypertens. 1998;7:413–7.CrossRefPubMed
32.
Chiao H, Kohda Y, McLeroy P, Craig L, Housini I, Star RA. Alpha-melanocyte-stimulating hormone protects against renal injury after ischemia in mice and rats. J Clin Invest. 1997;99:1165–72.CrossRefPubMedPubMedCentral
33.
Kwon TH, Frokiaer J, Fernandez-Llama P, Knepper MA, Nielsen S. Reduced abundance of aquaporins in rats with bilateral ischemia-induced acute renal failure: prevention by alpha-MSH. Am J Physiol. 1999;277:F413–27.PubMed
34.
Deng J, Kohda Y, Chiao H, Wang Y, Hu X, Hewitt SM, et al. Interleukin-10 inhibits ischemic and cisplatin-induced acute renal injury. Kidney Int. 2001;60:2118–28.CrossRefPubMed
35.
Gong H, Wang W, Kwon TH, Jonassen T, Li C, Ring T, et al. EPO and alpha-MSH prevent ischemia/reperfusion-induced down-regulation of AQPs and sodium transporters in rat kidney. Kidney Int. 2004;66:683–95.CrossRefPubMed
36.
Hoke TS, Douglas IS, Klein CL, He Z, Fang W, Thurman JM, et al. Acute renal failure after bilateral nephrectomy is associated with cytokine-mediated pulmonary injury. J Am Soc Nephrol. 2007;18:155–64.CrossRefPubMed
37.
Klein CL, Hoke TS, Fang WF, Altmann CJ, Douglas IS, Faubel S. Interleukin-6 mediates lung injury following ischemic acute kidney injury or bilateral nephrectomy. Kidney Int. 2008;74:901–9.CrossRefPubMed
38.
Hassoun HT, Grigoryev DN, Lie ML, Liu M, Cheadle C, Tuder RM, et al. Ischemic acute kidney injury induces a distant organ functional and genomic response distinguishable from bilateral nephrectomy. Am J Physiol Renal Physiol. 2007;293:F30–40.CrossRefPubMed
39.
Grigoryev DN, Liu M, Hassoun HT, Cheadle C, Barnes KC, Rabb H. The local and systemic inflammatory transcriptome after acute kidney injury. J Am Soc Nephrol. 2008;19:547–58.CrossRefPubMedPubMedCentral
40.
Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, et al. Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int. 2009;75:689–98.CrossRefPubMedPubMedCentral
41.
42.
Belaaouaj A, Kim KS, Shapiro SD. Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science. 2000;289:1185–8.CrossRefPubMed
43.
Chua F, Laurent GJ. Neutrophil elastase: mediator of extracellular matrix destruction and accumulation. Proc Am Thorac Soc. 2006;3:424–7.CrossRefPubMed
44.
Ishii T, Doi K, Okamoto K, Imamura M, Dohi M, Yamamoto K, et al. Neutrophil elastase contributes to acute lung injury induced by bilateral nephrectomy. Am J Pathol. 2010;177:1665–73.CrossRefPubMedPubMedCentral
45.
Zeiher BG, Artigas A, Vincent JL, Dmitrienko A, Jackson K, Thompson BT, et al. Neutrophil elastase inhibition in acute lung injury: results of the STRIVE study. Crit Care Med. 2004;32:1695–702.CrossRefPubMed
46.
Akamoto S, Okano K, Sano T, Yachida S, Izuishi K, Usuki H, et al. Neutrophil elastase inhibitor (sivelestat) preserves antitumor immunity and reduces the inflammatory mediators associated with major surgery. Surg Today. 2007;37:359–65.CrossRefPubMed
47.
Inoue Y, Tanaka H, Ogura H, Ukai I, Fujita K, Hosotsubo H, et al. A neutrophil elastase inhibitor, sivelestat, improves leukocyte deformability in patients with acute lung injury. J Trauma. 2006;60:936–43. discussion 943.CrossRefPubMed
48.
Zarbock A, Schmolke M, Spieker T, Jurk K, Van Aken H, Singbartl K. Acute uremia but not renal inflammation attenuates aseptic acute lung injury: a critical role for uremic neutrophils. J Am Soc Nephrol. 2006;17:3124–31.CrossRefPubMed
49.
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. 2003;289:2104–12.CrossRefPubMed
50.
Hoag JB, Liu M, Easley RB, Britos-Bray MF, Kesari P, Hassoun H, et al. Effects of acid aspiration-induced acute lung injury on kidney function. Am J Physiol Renal Physiol. 2008;294:F900–8.CrossRefPubMed
51.
52.
Colletti LM, Kunkel SL, Walz A, Burdick MD, Kunkel RG, Wilke CA, et al. Chemokine expression during hepatic ischemia/reperfusion-induced lung injury in the rat. The role of epithelial neutrophil activating protein. J Clin Invest. 1995;95:134–41.CrossRefPubMedPubMedCentral
53.
Caty MG, Guice KS, Oldham KT, Remick DG, Kunkel SI. Evidence for tumor necrosis factor-induced pulmonary microvascular injury after intestinal ischemia-reperfusion injury. Ann Surg. 1990;212:694–700.CrossRefPubMedPubMedCentral
54.
Seekamp A, Mulligan MS, Till GO, Smith CW, Miyasaka M, Tamatani T, et al. Role of beta 2 integrins and ICAM-1 in lung injury following ischemia-reperfusion of rat hind limbs. Am J Pathol. 1993;143:464–72.PubMedPubMedCentral
55.
Dwivedi AJ, Wu R, Nguyen E, Higuchi S, Wang H, Krishnasastry K, et al. Adrenomedullin and adrenomedullin binding protein-1 prevent acute lung injury after gut ischemia-reperfusion. J Am Coll Surg. 2007;205:284–93.CrossRefPubMed
56.
Yost CS, Matthay MA, Gropper MA. Etiology of acute pulmonary edema during liver transplantation: a series of cases with analysis of the edema fluid. Chest. 2001;119:219–23.CrossRefPubMed
57.
Kostopanagiotou G, Routsi C, Smyrniotis V, Lekka ME, Kitsiouli E, Arkadopoulos N, et al. Alterations in bronchoalveolar lavage fluid during ischemia-induced acute hepatic failure in the pig. Hepatology. 2003;37:1130–8.CrossRefPubMed
58.
Colletti LM, Burtch GD, Remick DG, Kunkel SL, Strieter RM, Guice KS, et al. The production of tumor necrosis factor alpha and the development of a pulmonary capillary injury following hepatic ischemia/reperfusion. Transplantation. 1990;49:268–72.CrossRefPubMed
59.
Suzuki S, Nakamura S, Serizawa A, Sakaguchi T, Konno H, Muro H, et al. Role of Kupffer cells and the spleen in modulation of endotoxin-induced liver injury after partial hepatectomy. Hepatology. 1996;24:219–25.CrossRefPubMed
60.
Glasgow SC, Ramachandran S, Csontos KA, Jia J, Mohanakumar T, Chapman WC. Interleukin-1beta is prominent in the early pulmonary inflammatory response after hepatic injury. Surgery. 2005;138:64–70.CrossRefPubMed
61.
Alwall N, Lunderquist A, Olsson O. Studies on electrolyte-fluid retention. I. Uremic lung, fluid lung? On pathogenesis and therapy; a preliminary report. Acta Med Scand. 1953;146:157–63.CrossRefPubMed
62.
63.
Gibson DG. Haemodynamic factors in the development of acute pulmonary oedema in renal failure. Lancet. 1966;2:1217–20.CrossRefPubMed
Metadata
Title
Lung injury following acute kidney injury: kidney–lung crosstalk
Authors
Kent Doi
Tomoko Ishizu
Toshiro Fujita
Eisei Noiri
Publication date
01-08-2011
Publisher
Springer Japan
Published in
Clinical and Experimental Nephrology / Issue 4/2011
Print ISSN: 1342-1751
Electronic ISSN: 1437-7799
DOI
https://doi.org/10.1007/s10157-011-0459-4

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