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Am. J. Respir. Crit. Care Med., Volume 163, Number 6, May 2001, 1376-1383

Alveolar Fluid Clearance Is Impaired in the Majority of Patients with Acute Lung Injury and the Acute Respiratory Distress Syndrome

LORRAINE B. WARE and MICHAEL A. MATTHAY

Cardiovascular Research Institute and Departments of Medicine and Anesthesia, University of California, San Francisco, San Francisco, California

Because experimental studies have shown that intact alveolar epithelial fluid transport function is critical for resolution of pulmonary edema and acute lung injury, we measured net alveolar fluid clearance in 79 patients with acute lung injury or the acute respiratory distress syndrome. Pulmonary edema fluid and plasma were sampled serially in the first 4 hours after intubation. Net alveolar fluid clearance was calculated from sequential edema fluid protein measurements. Mean alveolar fluid clearance was 6%/h. Of the patients, 56% had impaired alveolar fluid clearance (< 3%/h), 32% had submaximal clearance (>=  3%/h, < 14%/h), and 13% had maximal clearance (>=  14%/h). These findings are contrasted to our recent report of 65 patients with hydrostatic pulmonary edema, in whom mean alveolar fluid clearance was 13%/h; only 25% had impaired clearance whereas 75% had submaximal or maximal clearance (J Appl Physiol 1999;87:1301-1312). Acute lung injury with maximal alveolar fluid clearance were more likely to be female (p = 0.03), and less likely to have sepsis (p = 0.01). Endogenous and exogenous catecholamines did not correlate with alveolar fluid clearance. Patients with maximal alveolar fluid clearance had significantly lower mortality and a shorter duration of mechanical ventilation. In summary, in contrast to hydrostatic pulmonary edema, alveolar fluid clearance in patients with acute lung injury and the acute respiratory distress syndrome is impaired in the majority of patients, and maximal alveolar fluid clearance is associated with better clinical outcomes.




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Am. J. Respir. Cell Mol. Biol., November 1, 2005; 33(5): 432 - 437.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
G. M. Mutlu and J. I. Sznajder
Mechanisms of pulmonary edema clearance
Am J Physiol Lung Cell Mol Physiol, November 1, 2005; 289(5): L685 - L695.
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 Am. J. Respir. Cell Mol. Bio.Home page
M. A. Matthay and G. A. Zimmerman
Acute Lung Injury and the Acute Respiratory Distress Syndrome: Four Decades of Inquiry into Pathogenesis and Rational Management
Am. J. Respir. Cell Mol. Biol., October 1, 2005; 33(4): 319 - 327.
[Full Text] [PDF]

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 Proc Am Thorac SocHome page
M. A. Matthay, L. Robriquet, and X. Fang
Alveolar Epithelium: Role in Lung Fluid Balance and Acute Lung Injury
Proceedings of the ATS, October 1, 2005; 2(3): 206 - 213.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
T. R. Martin, N. Hagimoto, M. Nakamura, and G. Matute-Bello
Apoptosis and Epithelial Injury in the Lungs
Proceedings of the ATS, October 1, 2005; 2(3): 214 - 220.
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G. Matute-Bello, J. S. Lee, W. C. Liles, C. W. Frevert, S. Mongovin, V. Wong, K. Ballman, S. Sutlief, and T. R. Martin
Fas-Mediated Acute Lung Injury Requires Fas Expression on Nonmyeloid Cells of the Lung
J. Immunol., September 15, 2005; 175(6): 4069 - 4075.
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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
M. R. Looney, C. Sartori, S. Chakraborty, P. F. James, J. B. Lingrel, and M. A. Matthay
Decreased expression of both the {alpha}1- and {alpha}2-subunits of the Na-K-ATPase reduces maximal alveolar epithelial fluid clearance
Am J Physiol Lung Cell Mol Physiol, July 1, 2005; 289(1): L104 - L110.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
P. M. Myrianthefs, A. Briva, E. Lecuona, V. Dumasius, D. H. Rutschman, K. M. Ridge, G. J. Baltopoulos, and J. I. Sznajder
Hypocapnic but Not Metabolic Alkalosis Impairs Alveolar Fluid Reabsorption
Am. J. Respir. Crit. Care Med., June 1, 2005; 171(11): 1267 - 1271.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Roux, H. Kawakatsu, B. Gartland, M. Pespeni, D. Sheppard, M. A. Matthay, C. M. Canessa, and J.-F. Pittet
Interleukin-1{beta} Decreases Expression of the Epithelial Sodium Channel {alpha}-Subunit in Alveolar Epithelial Cells via a p38 MAPK-dependent Signaling Pathway
J. Biol. Chem., May 13, 2005; 280(19): 18579 - 18589.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
V. Swystun, L. Chen, P. Factor, B. Siroky, P. D. Bell, and S. Matalon
Apical trypsin increases ion transport and resistance by a phospholipase C-dependent rise of Ca2+
Am J Physiol Lung Cell Mol Physiol, May 1, 2005; 288(5): L820 - L830.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
S. Matalon and H.-L. Ji
Oleic Acid Damages Ion Transport and Promotes Alveolar Edema: The Dark Side of Healthy Living
Am. J. Respir. Crit. Care Med., March 1, 2005; 171(5): 424 - 425.
[Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
G. M. Mutlu, W. J. Koch, and P. Factor
Alveolar Epithelial {beta}2-Adrenergic Receptors: Their Role in Regulation of Alveolar Active Sodium Transport
Am. J. Respir. Crit. Care Med., December 15, 2004; 170(12): 1270 - 1275.
[Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
D. Mehta, J. Bhattacharya, M. A. Matthay, and A. B. Malik
Integrated control of lung fluid balance
Am J Physiol Lung Cell Mol Physiol, December 1, 2004; 287(6): L1081 - L1090.
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X. Li, R. Shu, G. Filippatos, and B. D. Uhal
Apoptosis in lung injury and remodeling
J Appl Physiol, October 1, 2004; 97(4): 1535 - 1542.
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 Am. J. Pathol.Home page
T. Nakagomi, O. Kitada, K. Kuribayashi, H. Yoshikawa, K. Ozawa, S. Ogawa, and T. Matsuyama
The 150-Kilodalton Oxygen-Regulated Protein Ameliorates Lipopolysaccharide-Induced Acute Lung Injury in Mice
Am. J. Pathol., October 1, 2004; 165(4): 1279 - 1288.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
A. Krupa, H. Kato, M. A. Matthay, and A. K. Kurdowska
Proinflammatory activity of anti-IL-8 autoantibody:IL-8 complexes in alveolar edema fluid from patients with acute lung injury
Am J Physiol Lung Cell Mol Physiol, June 1, 2004; 286(6): L1105 - L1113.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
T. Sakuma, Y. Zhao, M. Sugita, M. Sagawa, H. Toga, T. Ishibashi, M. Nishio, and M. A. Matthay
Malnutrition impairs alveolar fluid clearance in rat lungs
Am J Physiol Lung Cell Mol Physiol, June 1, 2004; 286(6): L1268 - L1274.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
Y. Adir, Z. S. Azzam, E. Lecuona, S. Leal, L. Pesce, V. Dumasius, A. M. Bertorello, P. Factor, J. B. Young, K. M. Ridge, et al.
Augmentation of Endogenous Dopamine Production Increases Lung Liquid Clearance
Am. J. Respir. Crit. Care Med., March 15, 2004; 169(6): 757 - 763.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
M. Quintel, P. Pelosi, P. Caironi, J. P. Meinhardt, T. Luecke, P. Herrmann, P. Taccone, C. Rylander, F. Valenza, E. Carlesso, et al.
An Increase of Abdominal Pressure Increases Pulmonary Edema in Oleic Acid-induced Lung Injury
Am. J. Respir. Crit. Care Med., February 15, 2004; 169(4): 534 - 541.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
L. B. Ware
Modulation of Alveolar Fluid Clearance by Acute Inflammation: The Plot Thickens
Am. J. Respir. Crit. Care Med., February 1, 2004; 169(3): 332 - 333.
[Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
D. E. Sloniewsky, K. M. Ridge, Y. Adir, F. P. Fries, A. Briva, J. I. Sznajder, and P. H. S. Sporn
Leukotriene D4 Activates Alveolar Epithelial Na,K-ATPase and Increases Alveolar Fluid Clearance
Am. J. Respir. Crit. Care Med., February 1, 2004; 169(3): 407 - 412.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
X. Han, M. P. Fink, T. Uchiyama, R. Yang, and R. L. Delude
Increased iNOS activity is essential for pulmonary epithelial tight junction dysfunction in endotoxemic mice
Am J Physiol Lung Cell Mol Physiol, February 1, 2004; 286(2): L259 - L267.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
A. Pelaez, R. I. Bechara, P. C. Joshi, L. A. S. Brown, and D. M. Guidot
Granulocyte/macrophage colony-stimulating factor treatment improves alveolar epithelial barrier function in alcoholic rat lung
Am J Physiol Lung Cell Mol Physiol, January 1, 2004; 286(1): L106 - L111.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
I. C. Davis, W. M. Sullender, J. M. Hickman-Davis, J. R. Lindsey, and S. Matalon
Nucleotide-mediated inhibition of alveolar fluid clearance in BALB/c mice after respiratory syncytial virus infection
Am J Physiol Lung Cell Mol Physiol, January 1, 2004; 286(1): L112 - L120.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
G. Saumon
Pump and Circumstances
Am. J. Respir. Crit. Care Med., December 15, 2003; 168(12): 1408 - 1409.
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J. Frank, J. Roux, H. Kawakatsu, G. Su, A. Dagenais, Y. Berthiaume, M. Howard, C. M. Canessa, X. Fang, D. Sheppard, et al.
Transforming Growth Factor-{beta}1 Decreases Expression of the Epithelial Sodium Channel {alpha}ENaC and Alveolar Epithelial Vectorial Sodium and Fluid Transport via an ERK1/2-dependent Mechanism
J. Biol. Chem., November 7, 2003; 278(45): 43939 - 43950.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
Y. Berthiaume
Tumor Necrosis Factor and Lung Edema Clearance: The Tip of the Iceberg?
Am. J. Respir. Crit. Care Med., November 1, 2003; 168(9): 1022 - 1023.
[Full Text]

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 Am. J. Respir. Crit. Care Med.Home page
N. Elia, M. Tapponnier, M. A. Matthay, J. Hamacher, J.-C. Pache, M.-A. Brundler, M. Totsch, P. De Baetselier, L. Fransen, N. Fukuda, et al.
Functional Identification of the Alveolar Edema Reabsorption Activity of Murine Tumor Necrosis Factor-{alpha}
Am. J. Respir. Crit. Care Med., November 1, 2003; 168(9): 1043 - 1050.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
Y. Berthiaume
Long-term stimulation of alveolar epithelial cells by {beta}-adrenergic agonists: increased Na+ transport and modulation of cell growth?
Am J Physiol Lung Cell Mol Physiol, October 1, 2003; 285(4): L798 - L801.
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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
P. Prabhakaran, L. B. Ware, K. E. White, M. T. Cross, M. A. Matthay, and M. A. Olman
Elevated levels of plasminogen activator inhibitor-1 in pulmonary edema fluid are associated with mortality in acute lung injury
Am J Physiol Lung Cell Mol Physiol, July 1, 2003; 285(1): L20 - L28.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
M. Sugita, P. Ferraro, A. Dagenais, M.-E. Clermont, P. Barbry, R. P. Michel, and Y. Berthiaume
Alveolar Liquid Clearance and Sodium Channel Expression Are Decreased in Transplanted Canine Lungs
Am. J. Respir. Crit. Care Med., May 15, 2003; 167(10): 1440 - 1450.
[Abstract] [Full Text] [PDF]

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N. P. Mason, M. Petersen, C. Melot, B. Imanow, O. Matveykine, M.-T. Gautier, A. Sarybaev, A. Aldashev, M. M. Mirrakhimov, B. H. Brown, et al.
Serial changes in nasal potential difference and lung electrical impedance tomography at high altitude
J Appl Physiol, May 1, 2003; 94(5): 2043 - 2050.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
J. A. Frank, J.-F. Pittet, H. Lee, M. Godzich, and M. A. Matthay
High tidal volume ventilation induces NOS2 and impairs cAMP- dependent air space fluid clearance
Am J Physiol Lung Cell Mol Physiol, May 1, 2003; 284(5): L791 - L798.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
D. E. Schraufnagel, N. P. Agaram, A. Faruqui, S. Jain, L. Jain, K. M. Ridge, and J. I. Sznajder
Pulmonary lymphatics and edema accumulation after brief lung injury
Am J Physiol Lung Cell Mol Physiol, May 1, 2003; 284(5): L891 - L897.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
A. P. Comellas, L. M. Pesce, Z. Azzam, F. J. Saldias, and J. I. Sznajder
Scorpion Venom Decreases Lung Liquid Clearance in Rats
Am. J. Respir. Crit. Care Med., April 15, 2003; 167(8): 1064 - 1067.
[Abstract] [Full Text] [PDF]


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