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Clinical Investigations: LABORATORY MEASUREMENTS |

“Ultrasound Comet-Tail Images”: A Marker Of Pulmonary Edema*: A Comparative Study With Wedge Pressure And Extravascular Lung Water FREE TO VIEW

Eustachio Agricola, MD; Tiziana Bove, MD; Michele Oppizzi, MD; Giovanni Marino, MD; Alberto Zangrillo, MD; Alberto Margonato, MD; Eugenio Picano, MD
Author and Funding Information

*From the Divisions of Non-Invasive Cardiology (Drs. Agricola, Oppizzi, and Margonato) and Anesthesiology and Intensive Care (Drs. Bove, Marino, and Zangrillo), Cardiothoracic Department, San Raffaele Hospital, Istituto di Richerche e Cura a carattere Scientifico, Milano; and Institute of Clinical Physiology (Dr. Picano), Consiglio Nazionale delle Richerche, Pisa, Italy.

Correspondence to: Eustachio Agricola, MD, Division of Non-Invasive Cardiology, Cardiothoracic Department, San Raffaele Hospital, IRCCS, Via Olgettina 60, 20132 Milano, Italy; e-mail: agricola.eustachio@hsr.it



Chest. 2005;127(5):1690-1695. doi:10.1378/chest.127.5.1690
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Background: Echographic examination of the lung surface may reveal multiple “comet-tail images” originating from water-thickened interlobular septa. These images could be useful for noninvasive assessment of interstitial pulmonary edema.

Study objective: The purpose of this study was to assess the diagnostic accuracy of lung comet-tail images compared with chest radiography, wedge pressure, and extravascular lung water (EVLW) quantified by the indicator dilution method (PiCCO System, version 4.1; Pulsion Medical Systems; Munich, Germany).

Methods and patients: We enrolled 20 patients (mean age, 62.6 ± 11.5 years [± SD]). Patients were studied before, immediately after, and 24 h following cardiac surgery with chest ultrasound, chest radiography, pulmonary artery catheterization, and the PiCCO system. Performing echo scanning (right and left hemithorax, from second to fourth intercostal space, from parasternal to midaxillary line), an individual patient comet score was obtained by summing the number of comets in each scanned space.

Results: A total of 60 comparisons were obtained. Significant positive linear correlations were found between comet score and EVLW determined by the PiCCO System (r = 0.42, p = 0.001), between comet score and wedge pressure (r = 0.48, p = 0.01), and between comet score and radiologic lung water score (r = 0.60, p = 0.0001).

Conclusions: The presence and the number of comet-tail images provide reliable information on interstitial pulmonary edema. Therefore, ultrasonography represent an attractive, easy-to-use, bedside diagnostic tool for assessing cardiac function and pulmonary congestion.

Figures in this Article

The objective diagnosis of interstitial pulmonary edema is traditionally based on chest radiographic findings, which when performed at the bedside may be difficult to interpret, and can have weak correlations with extravascular lung water (EVLW).12 The lung is considered poorly accessible using ultrasound because air prevents the progression of the ultrasound beam with production of reverberation artifacts under the lung surface.3The “comet-tail image” is an echographic image detectable with a cardiac ultrasound probe positioned over the chest.4 This image consists of multiple comet tails fanning out from the lung surface originating from water-thickened interlobular septa, and could provide useful information on EVLW.

The correlation between comet-tail images and interstitial edema has been documented by CT scanning,56 but not validated by quantitative measurements of EVLW.78 The purpose of this study was to assess the correlation between lung comet-tail images with chest radiographic findings, wedge pressure, and EVLW measured by the indicator dilution method (PiCCO System, version 4.1; Pulsion Medical Systems; Munich, Germany).

Patients

We enrolled 20 patients (16 men and 4 women; mean age, 62.6 ± 11.5 years) who underwent cardiac surgery with cardiopulmonary bypass (Table 1 ). Patients with lung diseases were excluded. The patients were assessed with chest ultrasonography, chest radiography, pulmonary artery catheterization, and the PiCCO System at baseline, immediately after surgical operation, and after 24 h. All examinations were performed within a few minutes and were read by independent operators unaware of the results of the other tests. All patients gave their informed consent.

Chest Ultrasound

The echographic examinations were performed with patients in the supine position. The ultrasound scanning of the anterior and lateral chest was obtained on both the right and left hemithorax, the second to fourth (on the right side to the fifth) intercostal space, and the parasternal to midaxillary line. In each intercostal space, the number of comet-tail images was registered at the parasternal, midclavear, anterior, and middle axillary lines as previously described.9 The sum of the comet-tail images was provided as an echo comet score of the extravascular fluid of the lung. Zero was defined as a complete absence of comet-tail images on the investigated area. The intraobserver and interobserver variabilities of the echo comet score were assessed by two independent observers (E.A. and T.B.) in a set of 10 consecutive cases, and were 3.1% and 4.4%, respectively. The comet-tail image was defined as a hyperechogenic, coherent bundle with narrow basis spreading from the transducer to the further border of the screen.56 The comet-tail image described here extends to the edge of the screen (whereas short comet-tail artifacts may exist in other regions), and arises only from the pleural line.6 Comet-tail images arising from the pleural line can be localized or disseminated to the whole lung surface, or again isolated or multiple (when at least three artifacts are visible in a frozen image in one longitudinal scan), with a distance ≤ 7 mm between two artifacts) [Fig 1 , top, A].,6 A positive (or pathologic) test result was defined as bilateral multiple comet-tail images, either disseminated (defined as all over the anterolateral lung surface) or lateral (defined as limited to the lateral lung surface). A negative test result was defined as an absence of comet-tail images, replaced by the horizontal artifact (Fig 1, bottom, B), or when rare, isolated comet-tail images were visible or when multiple comet-tail images were confined laterally to the last intercostal space above the diaphragm.,6 The examinations were performed using an ultrasound system (Sonos 5500; Phillips Medical Systems; Andover, MA) equipped with 1.8- to 3.6-MHz probe.

Chest Radiography

The patients underwent chest radiography in the supine position with specific assessment of EVLW using a commercially available radiograph machine and a standard technique. A previously validated radiologic score of EVLW was used incorporating assessment of hilar vessels (dimension, density, blurring), Kerley lines (A, B, and C), micronoduli, widening of interlobar fissures, peribronchial and perivascular cuffs, subpleural effusion, and diffuse increase in density (Table 2 ).1012 The intraobserver and interobserver reproducibility of radiologic scoring of EVLW among experienced observers was very high, as previously described.1012

PiCCO System

The PiCCO System is a device for cardiac output (CO) measurement combined with cardiac preload volume and lung water monitoring. It computes the CO utilizing an arterial pulse contour analysis algorithm after calibration by means of a transpulmonary thermodilution method.

In all patients, a 5F thermistor-tipped catheter (Pulsiocath PV8115; Pulsion Medical Systems) was placed into the right femoral artery, and connected to the PiCCO System for monitoring. To calibrate this system, individual arterial input impedance to arterial pressure is calculated by simultaneously determining the area under the systolic portion of the arterial pulse wave. A 10-mL bolus of cold 5% dextrose solution is injected through central venous catheter, and the thermodilution curve is evaluated with arterial catheter inserted in the femoral artery. The mean of three consecutive boluses was used. If an injection had to be rejected, more injections were made to obtain three measurements after rejecting the lowest and the highest value. From the CO we can obtain the intrathoracic thermal volume and the intrathoracic blood volume; from the difference of these two parameters, we can obtain the value of EVLW. Normally, EVLW is < 500 mL1315; the alveolar flooding appears usually when the EVLW is > 75% above normal limit.1516

Pulmonary Artery Pressure

A pulmonary artery catheter was introduced via the right internal jugular vein for conventional pulmonary artery thermodilution CO measurements. Pulmonary wedge pressure, and systolic, diastolic, and mean pulmonary pressures were also measured.

Statistical Analysis

Data are expressed as the mean value ± SD or percentages. The correlations between echo comet score, EVLW, radiologic lung water score, and data obtained by pulmonary artery catheter monitoring were analyzed by the Pearson two-tailed method. Moreover, the agreement between chest ultrasound and radiograph methods was analyzed using the Bland and Altman method.17 Bias between the methods was calculated as the mean difference between echo comet score and radiograph score. The upper and the lower limits of agreement were calculated as bias (2 SD), and defined the range in which 95% of the differences between the methods were expected to lie. The precision of the bias analysis and limits of agreement was assessed using 95% confidence intervals. Bias between comet score and radiograph score was analyzed using the paired Student t test. The difference in the mean content of EVLW between positive and negative comet test results was evaluated with an independent Student t test. Moreover, we calculated the sensitivity and specificity of a negative test result for detection of EVLW content < 500 mL, the sensitivity and specificity of a positive test for detection of EVLW content > 500 mL, and finally the sensitivity and specificity of a positive test result for detection an excess of EVLW below the threshold of alveolar flooding. A p value < 0.05 was considered statistically significant. The statistical analysis was performed using software (version 8.0; SPSS; Chicago, IL).

The determinations with the different methods were obtained in all patients. No data were rejected. A total of 60 comparative measurements were performed between the methods.

Comparison Between Chest Ultrasound, Chest Radiograph Findings, and EVLW

The feasibility of the chest ultrasound examination for the diagnosis of EVLW was 100%. The time needed for the echo lung examination was < 5 min in all cases (mean, 4.3 ± 1 min). The mean number of comets per person (comet score) was 7.6 ± 9.3, the mean radiologic score was 12 ± 7, and the mean EVLW was 643.7 ± 603.6 mL.

A significant positive linear correlation was found between echo comet score and radiologic score (r = 0.60, p < 0.0001), and no significant difference in the mean difference between these two scores was observed (bias, 4.7; 95% limits of agreement, − 9.9 to 19.3). There was a significant positive linear correlation between echo comet score and EVLW (r = 0.42, p = 0.001) [Fig 2] .

Comparison Between Chest Ultrasound and Hemodynamic Parameters

Positive linear correlations were found between echo comet score and wedge pressure (r = 0.48, p < 0.0001) and systolic pulmonary pressure (r = 0.53, p = 0.007) determined using pulmonary artery catheterization (Fig 3 ). No significant correlations between echo comet score and CO and cardiac index were observed.

Positive vs Negative Comet Test Results

Thirty-two examination results were considered positive and 28 were negative. When we compared the group of test results considered positive vs negative, a significant difference in mean EVLW was found (742 ± 277 mL vs 392 ± 92 mL, p = 0.0001). The mean content of EVLW in negative test result was below the normal limit of EVLW (< 500 mL). The sensitivity and specificity of the negative test result for detection of a content of EVLW < 500 mL were 90% and 89% respectively, whereas the sensitivity and specificity of the positive test result for detection of a content of EVLW > 500 mL, which is associated with pulmonary edema, were 90% and 86%, respectively. Finally, a positive test result had a sensitivity and specificity to detect an excess of EVLW below the threshold of alveolar edema of 87% and 89%, respectively.

The present study shows that the lung comet-tail images are correlated with wedge pressure and EVLW. Thus, their presence and number permit quantification of the excess of EVLW, providing an indirect measurement of wedge pressure. Moreover, it is sufficiently sensitive and accurate to detect pulmonary interstitial edema even before it becomes apparent clinically.

The comet-tail images appear when there is a marked difference in acoustic impedance between an object and its surroundings.4 The reflection of the beam creates a phenomenon of resonance. The time lag between successive reverberations is interpreted as a distance, resulting in a center that behaves like a persistent source, generating a series of very closely spaced pseudo-interfaces4(Fig 1, top, A). A normal lung contains much air and little water on the lung surface, so with ultrasounds no dense structures are visible in normal subjects. The normal ultrasound lung pattern is characterized by roughly horizontal, parallel lines (Fig 1, bottom, B), whereas pulmonary interstitial edema yields roughly vertical, parallel lines.6 The comet-tail image is related to a small water-rich structure, below the resolution of the ultrasound beam surrounded by air, and this element has to be present at the surface of the lung.5 Subpleural interlobular septa thickened by edema perfectly combine all of these properties as confirmed by CT correlations study.5 The subpleural end of a thickened septum is too thin to be visualized by the ultrasound beam, but it is thick enough to “disturb” the beam and create a difference in acoustic impedance with the surrounding air. Another type of lesion is associated with the artifact: ground-glass areas, which by creating a close mingling of small air-filled and liquid-filled areas, may produce the impedance gradient.5

According to the present study, chest ultrasound has potential to identify and quantify radiologically assessed EVLW; this is especially true if we consider that there is a significant correlation between echo comet score and the EVLW measured with PiCCO System. Usually, chest radiographs allow adequate recognition of pulmonary edema, with signs evolving as a function of the wedge pressure.18However the correlation between radiologic signs of pulmonary edema and wedge pressure may be approximate.19 Pulmonary edema with high wedge pressure can coexist with paucity or absence of radiologic signs of pulmonary edema,19 whereas in the present study we found a positive linear correlations between echo comet score and wedge pressure; therefore, the number of comet-tail images can provide an indirect measurement of wedge pressure. This turns into an advantage because these images are detectable at a very early stage of pulmonary edema, appearing below the threshold of alveolar edema.56 In fact, alveolar edema is always preceded by interstitial edema, a constant feature of pulmonary edema, the radiologic diagnosis of which is difficult at bedside.20 Moreover, most imaging methods do not estimate EVLW per se, but instead produce estimates of total water content (ie, vascular plus extravascular water),,15 whereas the chest ultrasound provides an estimate of only EVLW. Finally, we found a good value of sensitivity and specificity of the negative test result for detection of a content EVLW < 500 mL, confirming that the pattern of rare, isolated comet-tail images or confined laterally to the last intercostal space above the diaphragm must be considered as false-positive results.5

Bedside chest ultrasound has numerous clinical advantages. Recognition of the comet-tail image provides immediate noninvasive information; it can be performed at bedside also with an unsophisticated hand-held device; it is very simple to interpret and easy to quantify; it is not dependent on cardiac acoustic window or patient decubitus; the learning curve is short; and due to the no-ionizing nature of the examination, it is useful in following up the patient over time and tailoring therapy.6 Furthermore, the possibility of obtaining information on EVLW with a very simple, bedside technology further expands the possibility of a diagnosis based on ultrasound for assessing both cardiac function and pulmonary congestion, which are the two fundamental parameters needed for primary diagnosis, serial follow-up, and therapy tailoring in heart failure patients.21

The present study has its limitations. We excluded patients with lung diseases. In this way, lung pathology may have been underrepresented in our series, reducing the possibility of false-positive results.56 Ultrasound detection of interstitial syndrome does not necessarily imply a cardiogenic origin: pneumonia, ARDS, chronic interstitial lung diseases, or third-space syndrome after cardiopulmonary bypass, as in our patients, can give comet-tail images.22 However, the aim of the present study was to validate the presence and the number of these images with a quantitative measurement of EVLW independently of the generating cause.

In conclusion, the analysis of the presence and the number of “sonographic Kerley lines” allowed us to detect and quantify pulmonary edema. The possibility of obtaining information on EVLW with simplicity and high feasibility with bedside technology makes the ultrasound an attractive and easy to use diagnostic tool at the bedside for assessing cardiac function and pulmonary congestion.

Abbreviations: CO = cardiac output; EVLW = extravascular lung water

Table Graphic Jump Location
Table 1. Clinical Features
* 

Data are presented as mean ± SD unless otherwise indicated.

Figure Jump LinkFigure 1. Top, A: Typical comet-tail artifacts: hyperechogenic, coherent vertical bundles with narrow basis spreading from the transducer to the further border of the screen. This artifact is composed of multiple microreflections of the ultrasound beam. Bottom, B: Normal subject, with regular, parallel, roughly horizontal hyperechogenic lines due to the lung-wall interface.Grahic Jump Location
Table Graphic Jump Location
Table 2. Radiologic Scoring of EVLW
* 

The score assigned to each variable depends on the severity of involvement: ie, Hilary vessels enlarged: 1, normal mild enlargement; 2, moderate enlargement; 3, severe enlargement.

Figure Jump LinkFigure 2. Significant positive linear correlation between comet score and EVLW determined with the indicator thermodilution method (PiCCO System).Grahic Jump Location
Figure Jump LinkFigure 3. Positive linear correlation between comet score and wedge pressure determined using the pulmonary artery catheter.Grahic Jump Location
Halperin, B, Feeley, T, Mihm, F, et al (1985) Evaluation of the portable chest roentgenogram for quantitating extravascular lung water in critically ill adults.Chest88,649-652. [CrossRef] [PubMed]
 
Eisenberg, PR, Hansbrough, JR, Anderson, D, et al A prospective study of lung water measurements during patient management in an intensive care unit.Am Rev Respir Dis1987;136,662-668. [CrossRef] [PubMed]
 
Targhetta, R, Chavagneaux, R, Bourgeois, JM, et al Sonographic approach to diagnosing pulmonary consolidation.J Ultrasound Med1992;11,667-672. [PubMed]
 
Ziskin, MC, Thickman, DI, Goldenberg, NJ, et al The comet tail artifact.J Ultrasound Med1982;1,1-7
 
Lichtenstein, D, Méziére, G, Biderman, P, et al The Comet-tail artifact: an ultrasound sign of alveolar-interstitial syndrome.Am J Respir Crit Care Med1997;156,1640-1646. [PubMed]
 
Lichtenstein, D, Méziére, G A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact.Intensive Care Med1998;24,133-1334
 
Sivak, ED, Wiedemann, HP Clinical measurement of extravascular lung water.Crit Care Clin1986;2,511-526. [PubMed]
 
Effros, RM Lung water measurements with the mean transit time approach.J Appl Physiol1985;59,673-683. [PubMed]
 
Jambrik, Z, Monti, S, Coppola, V, et al Usefulness of ultrasound lung comets as a nonradiologic sign of extravascular lung water.Am J Cardiol2004;93,1265-1270. [CrossRef] [PubMed]
 
Milne, EN, Pistolesi, M, Miniati, M, et al The radiologic distinction of cardiogenic and noncardiogenic edema.AJR Am J Roentgenol1985;144,879-894. [PubMed]
 
Miniati, M, Pistolesi, M, Milne, EN, et al Detection of lung edema.Crit Care Med1987;15,1146-1155. [CrossRef] [PubMed]
 
Pistolesi, M, Miniati, M, Milne, EN, et al Measurement of extravascular lung water.Intensive Care World1991;8,16-21. [PubMed]
 
Lewis, FR, Elings, VB, Sturm, JA Bedside measurement of lung water.J Surg Res1979;27,250-261. [CrossRef] [PubMed]
 
Sibbald, WJ, Warshawski, FJ, Short, AK, et al Clinical studies of measuring extravascular lung water by the thermal dye technique in critically ill patients.Chest1983;83,725-731. [CrossRef] [PubMed]
 
Lange, NR, Schuster, DP The measurement of lung water.Crit Care1999;3,R19-R24. [CrossRef] [PubMed]
 
Bongard, FS, Matthay, M, Mackersie, RC, et al Morphologic and physiologic correlates of increased extravascular lung water.Surgery1984;96,395-403. [PubMed]
 
Bland, JM, Altman, DG Statistical methods for assessing agreement between two methods of clinical measurements.Lancet1986;1,307-310. [PubMed]
 
Givertz, MM, Colucci, WS, Braunwald, E Clinical aspects of heart failure: high-output failure, pulmonary edema. Braunwald, E Zipes, DS Libby, P eds.Heart disease 6th ed.2001,545-546 WB Saunders. Philadelphia, PA:
 
Chakko, S, Woska, D, Martinez, H, et al Clinical, radiographic and hemodynamic correlations in congestive heart failure: conflicting results may lead to inappropriate care.Am J Med1991;90,353-359. [PubMed]
 
Staub, NC Pulmonary edema.Physiol Rev1974;54,678-811. [CrossRef] [PubMed]
 
Remme, WJ, Swedberg, K European Society of Cardiology. Comprehensive guidelines for the diagnosis and treatment of chronic heart failure. Task Force for the Diagnosis and Treatment of Chronic Heart Failure of the European Society of Cardiology.Eur J Heart Fail2002;4,11-22. [CrossRef] [PubMed]
 
Weiss, YG, Merin, G, Koganov, E, et al Postcardiopulmonary bypass hypoxemia: a prospective study of incidence, risk factor and clinical significance.J Cardiothorac Vasc Anesth2000;14,506-513. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1. Top, A: Typical comet-tail artifacts: hyperechogenic, coherent vertical bundles with narrow basis spreading from the transducer to the further border of the screen. This artifact is composed of multiple microreflections of the ultrasound beam. Bottom, B: Normal subject, with regular, parallel, roughly horizontal hyperechogenic lines due to the lung-wall interface.Grahic Jump Location
Figure Jump LinkFigure 2. Significant positive linear correlation between comet score and EVLW determined with the indicator thermodilution method (PiCCO System).Grahic Jump Location
Figure Jump LinkFigure 3. Positive linear correlation between comet score and wedge pressure determined using the pulmonary artery catheter.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Clinical Features
* 

Data are presented as mean ± SD unless otherwise indicated.

Table Graphic Jump Location
Table 2. Radiologic Scoring of EVLW
* 

The score assigned to each variable depends on the severity of involvement: ie, Hilary vessels enlarged: 1, normal mild enlargement; 2, moderate enlargement; 3, severe enlargement.

References

Halperin, B, Feeley, T, Mihm, F, et al (1985) Evaluation of the portable chest roentgenogram for quantitating extravascular lung water in critically ill adults.Chest88,649-652. [CrossRef] [PubMed]
 
Eisenberg, PR, Hansbrough, JR, Anderson, D, et al A prospective study of lung water measurements during patient management in an intensive care unit.Am Rev Respir Dis1987;136,662-668. [CrossRef] [PubMed]
 
Targhetta, R, Chavagneaux, R, Bourgeois, JM, et al Sonographic approach to diagnosing pulmonary consolidation.J Ultrasound Med1992;11,667-672. [PubMed]
 
Ziskin, MC, Thickman, DI, Goldenberg, NJ, et al The comet tail artifact.J Ultrasound Med1982;1,1-7
 
Lichtenstein, D, Méziére, G, Biderman, P, et al The Comet-tail artifact: an ultrasound sign of alveolar-interstitial syndrome.Am J Respir Crit Care Med1997;156,1640-1646. [PubMed]
 
Lichtenstein, D, Méziére, G A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact.Intensive Care Med1998;24,133-1334
 
Sivak, ED, Wiedemann, HP Clinical measurement of extravascular lung water.Crit Care Clin1986;2,511-526. [PubMed]
 
Effros, RM Lung water measurements with the mean transit time approach.J Appl Physiol1985;59,673-683. [PubMed]
 
Jambrik, Z, Monti, S, Coppola, V, et al Usefulness of ultrasound lung comets as a nonradiologic sign of extravascular lung water.Am J Cardiol2004;93,1265-1270. [CrossRef] [PubMed]
 
Milne, EN, Pistolesi, M, Miniati, M, et al The radiologic distinction of cardiogenic and noncardiogenic edema.AJR Am J Roentgenol1985;144,879-894. [PubMed]
 
Miniati, M, Pistolesi, M, Milne, EN, et al Detection of lung edema.Crit Care Med1987;15,1146-1155. [CrossRef] [PubMed]
 
Pistolesi, M, Miniati, M, Milne, EN, et al Measurement of extravascular lung water.Intensive Care World1991;8,16-21. [PubMed]
 
Lewis, FR, Elings, VB, Sturm, JA Bedside measurement of lung water.J Surg Res1979;27,250-261. [CrossRef] [PubMed]
 
Sibbald, WJ, Warshawski, FJ, Short, AK, et al Clinical studies of measuring extravascular lung water by the thermal dye technique in critically ill patients.Chest1983;83,725-731. [CrossRef] [PubMed]
 
Lange, NR, Schuster, DP The measurement of lung water.Crit Care1999;3,R19-R24. [CrossRef] [PubMed]
 
Bongard, FS, Matthay, M, Mackersie, RC, et al Morphologic and physiologic correlates of increased extravascular lung water.Surgery1984;96,395-403. [PubMed]
 
Bland, JM, Altman, DG Statistical methods for assessing agreement between two methods of clinical measurements.Lancet1986;1,307-310. [PubMed]
 
Givertz, MM, Colucci, WS, Braunwald, E Clinical aspects of heart failure: high-output failure, pulmonary edema. Braunwald, E Zipes, DS Libby, P eds.Heart disease 6th ed.2001,545-546 WB Saunders. Philadelphia, PA:
 
Chakko, S, Woska, D, Martinez, H, et al Clinical, radiographic and hemodynamic correlations in congestive heart failure: conflicting results may lead to inappropriate care.Am J Med1991;90,353-359. [PubMed]
 
Staub, NC Pulmonary edema.Physiol Rev1974;54,678-811. [CrossRef] [PubMed]
 
Remme, WJ, Swedberg, K European Society of Cardiology. Comprehensive guidelines for the diagnosis and treatment of chronic heart failure. Task Force for the Diagnosis and Treatment of Chronic Heart Failure of the European Society of Cardiology.Eur J Heart Fail2002;4,11-22. [CrossRef] [PubMed]
 
Weiss, YG, Merin, G, Koganov, E, et al Postcardiopulmonary bypass hypoxemia: a prospective study of incidence, risk factor and clinical significance.J Cardiothorac Vasc Anesth2000;14,506-513. [CrossRef] [PubMed]
 
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