Overview of the pathology of three widely used animal models of acute lung injury

European Surgical Research

Volumn 40, Issue 4, 2008, Pages 305-316

  Wang, H M ^a,b   Bodenstein, M ^a   Markstaller, K ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

Author keywords

Acute lung injury; Animal model; Endotoxin lipopolysaccharide; Lavage; Oleic acid; Pathology

Indexed keywords

LIPOPOLYSACCHARIDE; OLEIC ACID;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; DISEASE MODEL; LUNG LAVAGE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRONCHOALVEOLAR LAVAGE; DISEASE MODELS, ANIMAL; DOGS; HUMANS; LIPOPOLYSACCHARIDES; LUNG; OLEIC ACID; RESPIRATORY DISTRESS SYNDROME, ADULT; SHEEP; SWINE;

EID: 43949093848     PISSN: 0014312X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000121471     Document Type: Review

References (96)

1. Lee W, Downey G: Neutrophil activation and acute lung injury. Curr Opin Crit Care 2001;7:1-7.
2. Luh S, Chiang C: Acute lung injury/acute respiratory distress syndrome (ALI/ARDS): the mechanism, present strategies and future perspectives of therapies. J Zhejiang Univ Sci B 2007;8:60-69.
3. Windsor AC, Mullen PG, Fowler AA: Acute lung injury: what have we learned from animal models? Am J Med Sci 1993;306:111-116.
4. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, Lamy M, Legall J, Morris A, Spragg R: The American-European consensus conference on ARDS: definitions, mechanisms, relevant outcomes, and clinical coordination. Am J Respir Crit Care Med 1994;149:818-824.
5. Rocco PR, Zin WA: Pulmonary and extrapulmonary acute respiratory distress syndrome: are they different? Curr Opin Crit Care 2005;11:10-17.
6. Karmrodt J, Bletz C, Yuan S, David M, Heussel CP, Markstaller K: Quantification of atelectatic lung volumes in two different porcine models of ARDS. Br J Anaesth 2006;97:883-895.
7. Odenstedt H, Aneman A, Karason S, Stenqvist O, Lundin S: Acute hemodynamic changes during lung recruitment in lavage and endotoxin-induced ALI. Intensive Care Med 2005;31:112-120.
8. Lethvall S, Lindgren S, Lundin S, Stenqvist O: Tracheal double-lumen ventilation attenuates hypercapnia and respiratory acidosis in lung injured pigs. Intensive Care Med 2004;30:686-692.
9. Blanch L, Van der Kloot TE, Youngblood AM, Murias G, Naveira A, Adams AB, Romero PV, Nahum A: Application of tracheal gas insufflation to acute unilateral lung injury in an experimental model. Am J Respir Crit Care Med 2001;164:642-647.
10. Kloot TE, Blanch L, Melynne Youngblood A, Weinert C, Adams AB, Marini JJ, Shapiro RS, Nahum A: Recruitment maneuvers in three experimental models of acute lung injury: effect on lung volume and gas exchange. Am J Respir Crit Care Med 2000;161:1485-1494.
11. Musch G, Harris RS, Vidal Melo MF, O'Neill KR, Layfield JD, Winkler T, Venegas JG: Mechanism by which a sustained inflation can worsen oxygenation in acute lung injury. Anesthesiology 2004;100:323-330.
12. Kirmse M, Fujino Y, Hess D, Kacmarek RM: Positive end-expiratory pressure improves gas exchange and pulmonary mechanics during partial liquid ventilation. Am J Respir Crit Care Med 1998;158:1550-1556.
13. Fuchs JR, Kaviani A, Watson K, Thompson J, Wilson JM, Fauza DO: Intratracheal pulmonary ventilation improves gas exchange during laparoscopy in a pediatric lung injury model. J Pediatr Surg 2005;40:22-25.
14. Manaligod JM, Bendel-Stenzel EM, Meyers PA, Bing DR, Connett JE, Mammel MC: Variations in end-expiratory pressure during partial liquid ventilation: impact on gas exchange, lung compliance, and end-expiratory lung volume. Chest 2000;117:184-190.
15. Bellardine CL, Hoffman AM, Tsai L, Ingenito EP, Arold SP, Lutchen KR, Suki B: Comparison of variable and conventional ventilation in a sheep saline lavage lung injury model. Crit Care Med 2006;34:439-445.
16. Zick G, Frerichs I, Schadler D, Schmitz G, Pulletz S, Cavus E, Wachtler F, Scholz J, Weiler N: Oxygenation effect of interventional lung assist in a lavage model of acute lung injury: a prospective experimental study. Crit Care 2006;10:R56.
17. Kobayashi H, Tanaka N, Winkler M, Zapol WM: Combined effects of NO inhalation and intravenous PGF2 alpha on pulmonary circulation and gas exchange in an ovine ARDS model. Intensive Care Med 1996;22:656-663.
18. Bellardine Black CL, Hoffman AM, Tsai LW, Ingenito EP, Suki B, Kaczka DW, Simon BA, Lutchen KR: Relationship between dynamic respiratory mechanics and disease heterogeneity in sheep lavage injury. Crit Care Med 2007;35:870-878.
19. Dolan S, Derdak S, Solomon D, Farmer C, Johanningman J, Gelineau J, Smith RB: Tracheal gas insufflation combined with high-frequency oscillatory ventilation. Crit Care Med 1996;24:458-465.
20. Luecke T, Meinhardt JP, Herrmann P, Weiss A, Quintel M, Pelosi P: Oleic acid vs saline solution lung lavage-induced acute lung injury: effects on lung morphology, pressure-volume relationships, and response to positive end-expiratory pressure. Chest 2006;130:392-401.
21. Henzler D, Mahnken AH, Wildberger JE, Rossaint R, Gunther RW, Kuhlen R: Multislice spiral computed tomography to determine the effects of a recruitment maneuver in experimental lung injury. Eur Radiol 2006;16:1351-1359.
22. Greif WM, Forse RA: Cardiopulmonary effects of the laparoscopic pneumoperitoneum in a porcine model of adult respiratory distress syndrome. Am J Surg 1999;177:216-221.
23. Brederlau J, Muellenbach R, Kredel M, Kuestermann J, Anetseder M, Greim C, Roewer N: Combination of arteriovenous extracorporeal lung assist and high-frequency oscillatory ventilation in a porcine model of lavage-induced acute lung injury: a randomized controlled trial. J Trauma 2007;62:336-346.
24. Kredel M, Muellenbach RM, Brock RW, Wilckens HH, Brederlau J, Roewer N, Wunder C: Liver dysfunction after lung recruitment manoeuvres during pressure-controlled ventilation in experimental acute respiratory distress. Crit Care 2007;11:R13.
25. Ye SQ, Simon BA, Maloney JP, Zambelli-Weiner A, Gao L, Grant A, Easley RB, McVerry BJ, Tuder RM, Standiford T, Brower RG, Barnes KC, Garcia JG: Pre-B-cell colony-enhancing factor as a potential novel biomarker in acute lung injury. Am J Respir Crit Care Med 2005;171:361-370.
26. Claesson J, Lehtipalo S, Bergstrand U, Arnerlov C, Winso O: Negative mesenteric effects of lung recruitment maneuvers in oleic acid lung injury are transient and short lasting. Crit Care Med 2007;35:230-238.
27. Roch A, Michelet P, Lambert D, Delliaux S, Saby C, Perrin G, Ghez O, Bregeon F, Thomas P, Carpentier JP, Papazian L, Auffray JP: Accuracy of the double indicator method for measurement of extravascular lung water depends on the type of acute lung injury. Crit Care Med 2004;32:811-817.
28. Gust R, McCarthy TJ, Kozlowski J, Stephenson AH, Schuster DP: Response to inhaled nitric oxide in acute lung injury depends on distribution of pulmonary blood flow prior to its administration. Am J Respir Crit Care Med 1999;159:563-570.
29. Neumann P, Berglund JE, Mondejar EF, Magnusson A, Hedenstierna G: Effect of different pressure levels on the dynamics of lung collapse and recruitment in oleic-acid-induced lung injury. Am J Respir Crit Care Med 1998;158:1636-1643.
30. Zwissler B, Forst H, Ishii K, Messmer K: A new experimental model of ARDS and pulmonary hypertension in the dog. Res Exp Med (Berl) 1989;189:427-438.
31. Schweiger JW, Downs JB, Smith RA: Chest wall disruption with and without acute lung injury: effects of continuous positive airway pressure therapy on ventilation and perfusion relationships. Crit Care Med 2003;31:2364-2370.
32. Ludwigs U, Klingstedt C, Baehrendtz S, Wegenius G, Hedenstierna G: A functional and morphologic analysis of pressure-controlled inverse ratio ventilation in oleic acid-induced lung injury. Chest 1994;106:925-931.
33. Grotjohan HP, van der Heijde RM, Jansen JR, Wagenvoort CA, Versprille A: A stable model of respiratory distress by small injections of oleic acid in pigs. Intensive Care Med 1996;22:336-344.
34. Kirov MY, Kuzkov VV, Kuklin VN, Waerhaug K, Bjertnaes LJ: Extravascular lung water assessed by transpulmonary single thermodilution and postmortem gravimetry in sheep. Crit Care 2004;8:R451-R458.
35. Ragaller M, Bleyl J, Tscho U, Winkler T, Regner M, Rasche S, Koch T, Albrecht M: Effects of inhalation of perfluorocarbon aerosol on oxygenation and pulmonary function compared to PGI2 inhalation in a sheep model of oleic acid-induced lung injury. Intensive Care Med 2001;27:889-897.
36. Overbeck MC, Pranikoff T, Yadao CM, Hirschl RB: Efficacy of perfluorocarbon partial liquid ventilation in a large animal model of acute respiratory failure. Crit Care Med 1996;24:1208-1214.
37. Broccard AF, Shapiro RS, Schmitz LL, Ravenscraft SA, Marini JJ: Influence of prone position on the extent and distribution of lung injury in a high tidal volume oleic acid model of acute respiratory distress syndrome. Crit Care Med 1997;25:16-27.
38. Lee HJ, Im JG, Goo JM, Kim YI, Lee MW, Ryu HG, Bahk JH, Yoo CG: Acute lung injury: effects of prone positioning on cephalocaudal distribution of lung inflation - CT assessment in dogs. Radiology 2005;234:151-161.
39. Nieman GF, Gatto LA, Paskanik AM, Yang B, Fluck R, Picone A: Surfactant replacement in the treatment of sepsis-induced adult respiratory distress syndrome in pigs. Crit Care Med 1996;24:1025-1033.
40. Albertini M, Clement MG, Lafortuna CL, Caniatti M, Magder S, Abdulmalek K, Hussain SN: Role of poly-(ADP-ribose) synthetase in lipopolysaccharide- induced vascular failure and acute lung injury in pigs. J Crit Care 2000;15:73-83.
41. Pacht ER, Kindt GC, Lykens MG: Increased antioxidant activity in bronchoalveolar lavage fluid after acute lung injury in anesthetized sheep. Crit Care Med 1992;20:1441-1447.
42. Welsh C, Lien D, Worthen G, Weil J: Pentoxifylline decreases endotoxin-induced pulmonary neutrophil sequestration and extravascular protein accumulation in the dog. Am Rev Respir Dis 1988;138:1106-1114.
43. Da J, Chen L, Hedenstierna G: Nitric oxide up-regulates the glucocorticoid receptor and blunts the inflammatory reaction in porcine endotoxin sepsis. Crit Care Med 2007;35:26-32.
44. Maurenbrecher H, Lamy M, Deby-Dupont G, Frascarolo P, Hedenstierna G: An animal model of response and nonresponse to inhaled nitric oxide in endotoxin-induced lung injury. Chest 2001;120:573-581.
45. Dahm PL, Blomquist S, De Robertis E, Jonson B, Myhre E, Svantesson C, Thorne J: Effects of NO inhalation on pulmonary leukocyte sequestration and blood volume in porcine endotoxaemia. Intensive Care Med 2000;26:336-343.
46. Lutz C, Carney D, Finck C, Picone A, Gatto LA, Paskanik A, Langenback E, Nieman G: Aerosolized surfactant improves pulmonary function in endotoxin-induced lung injury. Am J Respir Crit Care Med 1998;158:840-845.
47. Modig J, Borg T: Biochemical markers in a porcine model of adult respiratory distress syndrome induced by endotoxemia. Resuscitation 1986;14:225-236.
48. Tabor DR, Kiel DP, Jacobs RF: Receptor-mediated ingestion responses by lung macrophages from a canine model of ARDS. J Leukoc Biol 1987;41:539-543.
49. Jacobs RF, Kiel DP, Balk RA: Alveolar macrophage function in a canine model of endotoxin-induced lung injury. Am Rev Respir Dis 1986;134:745-751.
50. Holm B, Matalon S: Role of pulmonary surfactant in the development and treatment of adult respiratory distress syndrome. Anesth Analg 1989;69:805-818.
51. Kuckelt W, Dauberschmidt R, Bender V, Hieronymi U, Mrochen H, Winsel K, Meyer M: Experimental investigations in adult respiratory distress syndrome (ARDS): repeated pulmonary lavage in LEWE-mini-pigs. I. Pulmonary mechanics, gas exchange, and pulmonary hemodynamics. Exp Pathol 1981;20:88-104.
52. Mallory G: Surfactant proteins: role in lung physiology and disease in early life. Paediatr Respir Rev 2001;2:151-158.
53. Vangerow B, Hafner D, Rueckoldt H, Marx G, Ott N, Leuwer M, Frerking I, Germann PG: Effects of C1 inhibitor and r-SP-C surfactant on oxygenation and histology in rats with lavage-induced acute lung injury. Intensive Care Med 2001;27:1526-1531.
54. Schuster DP: ARDS: clinical lessons from the oleic acid model of acute lung injury. Am J Respir Crit Care Med 1994;149:245-260.
55. Vadasz I, Morty RE, Kohstall MG, Olschewski A, Grimminger F, Seeger W, Ghofrani HA: Oleic acid inhibits alveolar fluid reabsorption: a role in acute respiratory distress syndrome? Am J Respir Crit Care Med 2005;171:469-479.
56. Ito K, Mizutani A, Kira S, Mori M, Iwasaka H, Noguchi T: Effect of Ulinastatin, a human urinary trypsin inhibitor, on the oleic acid-induced acute lung injury in rats via the inhibition of activated leukocytes. Injury 2005;36:387-394.
57. Chen J, Zhao J, Wang G: Preventive effects and mechanism of heme oxygenase-1 activation on acute respiratory distress syndrome in rats. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 2005;23:199-202.
58. Xu GL, Yao L, Rao SY, Gong ZN, Zhang SQ, Yu SQ: Attenuation of acute lung injury in mice by oxymatrine is associated with inhibition of phosphorylated p38 mitogen-activated protein kinase. J Ethnopharmacol 2005;98:177-183.
59. Nakazawa K, Yokoyama K, Yamakawa N, Makita K: Effect of positive end-expiratory pressure on inflammatory response in oleic acid-induced lung injury and whole-lung lavage-induced lung injury. J Anesth 2007;21:47-54.
60. Xie L, Liu Y, Zhao X, Chen L, Huang L, Hao F, Cao L: Effects of prone position ventilation on inflammatory factors in blood and bronchial alveolar lavage fluid of acute respiratory distress syndrome dogs caused by pulmonary and extrapulmonary insults. Zhonghua Yi Xue Za Zhi 2004;84:1200-1204.
61. Rosenthal C, Caronia C, Quinn C, Lugo N, Sagy M: A comparison among animal models of acute lung injury. Crit Care Med 1998;26:912-916.
62. Eiermann G, Dickey B, Thrall R: Polymorphonuclear leukocyte participation in acute oleic-acid-induced lung injury. Am Rev Respir Dis 1983;128:845-850.
63. Schoene R, Robertson H, Thorning D, Springmeyer S, Hlastala M, Cheney F: Pathophysiological patterns of resolution from acute oleic acid injury in the dog. J Appl Physiol 1984;56:472-481.
64. Ball H, Cook J, Spicer K, Wise W, Halushka P: Essential fatty acid-deficient rats are resistant to oleic acid-induced pulmonary injury. J Appl Physiol 1989;67:811-816.
65. Moriuchi H, Zaha M, Fukumoto T, Yuizono T: Activation of polymorphonuclear leukocytes in oleic acid-induced lung injury. Intensive Care Med 1998;24:709-715.
66. Julien M, Hoeffel J, Flick M: Oleic acid injury in sheep. J Appl Physiol 1986;60:433-440.
67. Hofman W, Ehrhart I: Permeability edema in dog lung depleted of blood components. J Appl Physiol 1984;57:147-153.
68. Golbidi S, Moriuchi H, Yang C, Irikura M, Irie T, Hamasaki N: Preventive effect of phosphoenolpyruvate on hypoxemia induced by oleic acid in guinea pigs. Biol Pharm Bull 2003;26:336-340.
69. B receptor-mediated mechanisms involved in oleic acid-induced acute lung injury in mice. Clin Sci (Lond) 2002;103(suppl 48):340S-344S.
70. Brigham KL, Meyrick B: Endotoxin and lung injury. Am Rev Respir Dis 1986;133:913-927.
71. Welbourn CR, Young Y: Endotoxin, septic shock and acute lung injury: neutrophils, macrophages and inflammatory mediators. Br J Surg 1992;79:998-1003.
72. Bannerman DD, Goldblum SE: Mechanisms of bacterial lipopolysaccharide- induced endothelial apoptosis. Am J Physiol Lung Cell Mol Physiol 2003;284:L899-L914.
73. Bhatia M, Moochhala S: Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J Pathol 2004;202:145-156.
74. Abraham E: Neutrophils and acute lung injury. Crit Care Med 2003;31(suppl 4):S195-S199.
75. Malhotra R, Bird M: L-selectin: a novel receptor for lipopolysaccharide and its potential role in bacterial sepsis. Bioessays 1997;19:919-923.
76. Monick M, Hunninghake G: Activation of second messenger pathways in alveolar macrophages by endotoxin. Eur Respir J 2002;20:210-222.
77. Kuebler W: Selectins revisited: the emerging role of platelets in inflammatory lung disease. J Clin Invest 2006;116:3106-3108.
78. Zarbock A, Singbartl K, Ley K: Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest 2006;116:3211-3219.
79. Jeyaseelan S, Chu H, Young S, Worthen G: Transcriptional profiling of lipopolysaccharide-induced acute lung injury. Infect Immun 2004;72:7247-7256.
80. Wang H, Yang H, Tracey K: Extracellular role of HMGB1 in inflammation and sepsis. J Intern Med 2004;255:320-331.
81. Siore AM, Parker RE, Stecenko AA, Cuppels C, McKean M, Christman BW, Cruz-Gervis R, Brigham KL: Endotoxin-induced acute lung injury requires interaction with the liver. Am J Physiol Lung Cell Mol Physiol 2005;289:L769-L776.
82. Huber G, Edmunds L, Finley T: Acute effect of saline lung washing on pulmonary mechanics and morphology. Surg Forum 1966;17:113-114.
83. Ashbaugh D, Uzawa T: Respiratory and hemodynamic changes after injection of free fatty acids. J Surg Res 1968;8:417-423.
84. King E, Nakane P, Ashbaugh D: The canine oleic acid model of fibrin localization in fat embolism. Surgery 1971;69:782-787.
85. Derks C, Jakobovitz-Derks D: Embolic pneumopathy induced by oleic acid: a systematic morphologic study. Am J Pathol 1977;87:143-158.
86. Miyazawa T, Nakagawa H, Hiramoto M, Arita K, Hiramoto T, Nishida O: Ultrastructural study on the alveolar-capillary injury with pulmonary edema induced by oleic acid in dogs. Hiroshima J Med Sci 1981;30:183-190.
87. Lutz CJ, Picone A, Gatto LA, Paskanik A, Landas S, Nieman GF: Exogenous surfactant and positive end-expiratory pressure in the treatment of endotoxin-induced lung injury. Crit Care Med 1998;26:1379-1389.
88. Sood SL, Balaraman V, Finn KC, Wilkerson SY, Mundie TG, Easa D: Exogenous surfactant decreases oxygenation in Escherichia coli endotoxin-treated neonatal piglets. Pediatr Pulmonol 1996;22:376-386.
89. Picone A, Gatto LA, Nieman GF, Paskanik AM, Lutz C: Pulmonary surfactant function following endotoxin: effects of exogenous surfactant treatment. Shock 1996;5:304-310.
90. Kemming G, Flondor M, Hanser A, Pallivathukal S, Holtmannspoetter M, Kneisel F, Reuter D, Kisch-Wedel H, Zwissler B: Effects of perfluorohexan vapor on gas exchange, respiratory mechanics, and lung histology in pigs with lung injury after endotoxin infusion. Anesthesiology 2005;103:585-594.
91. Müller-Leisse C, Klosterhalfen B, Hauptmann S, Simon H, Kashefi A, Andreopoulos D, Kirkpatrick C, Guenther R: Computed tomography and histologic results in the early stages of endotoxin-injured pig lungs as a model for adult respiratory distress syndrome. Invest Radiol 1993;28:39-45.
92. Meyrick B, Brigham K: Acute effects of E. coli endotoxin on the pulmonary microcirculation of anesthetized sheep: structure and function relationships. Lab Invest 1983;48:458-470.
93. Wheeler A, Bernard G: Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 2007;369:1553-1564.
94. Ware L, Matthay M: The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349.
95. Matute-Bello G, Martin T: Science review: apoptosis in acute lung injury. Crit Care 2003;7:355-358.
96. Mantell L, Kazzaz J, Xu J, Palaia T, Piedboeuf B, Hall S, Rhodes G, Niu G, Fein A, Horowitz S: Unscheduled apoptosis during acute inflammatory lung injury. Cell Death Differ 1997;4:600-607.