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Original Research: CHEST IMAGING |

Chest Ultrasonography for the Diagnosis and Monitoring of High-Altitude Pulmonary Edema* FREE TO VIEW

Peter J. Fagenholz, MD; Jonathan A. Gutman, MD; Alice F. Murray, MBChB; Vicki E. Noble, MD; Stephen H. Thomas, MD, MPH; N. Stuart Harris, MD, MFA
Author and Funding Information

*From the Departments of Surgery (Dr. Fagenholz) and Emergency Medicine (Drs. Harris, Noble, and Thomas), Massachusetts General Hospital, Harvard Medical School, Boston, MA; University of Washington (Dr. Gutman), Fred Hutchinson Cancer Research Center, Seattle, WA; and Emergency Department (Dr. Murray), Edinburgh Royal Infirmary, Edinburgh, Scotland, UK.

Correspondence to: N. Stuart Harris, MD, MFA, Department of Emergency Medicine, Clinics 115, Massachusetts General Hospital, 55 Fruit St, Boston, MA 02140; e-mail: nsharris@partners.org



Chest. 2007;131(4):1013-1018. doi:10.1378/chest.06-1864
Text Size: A A A
Published online

Background: The comet-tail technique of chest ultrasonography has been described for the diagnosis of cardiogenic pulmonary edema. This is the first report describing its use for the diagnosis and monitoring of high-altitude pulmonary edema (HAPE), the leading cause of death from altitude illness.

Methods: Eleven consecutive patients presenting to the Himalayan Rescue Association clinic in Pheriche, Nepal (4,240 m) with a clinical diagnosis of HAPE underwent one to three chest ultrasound examinations using the comet-tail technique to determine the presence of extravascular lung water (EVLW). Seven patients with no evidence of HAPE or other altitude illness served as control subjects. All examinations were read by a blinded observer.

Results: HAPE patients had higher comet-tail score (CTS) [mean ± SD, 31 ± 11 vs 0.86 ± 0.83] and lower oxygen saturation (O2Sat) [61 ± 9.2% vs 87 ± 2.8%] than control subjects (p < 0.001 for both). Mean CTS was higher (35 ± 11 vs 12 ± 6.8, p < 0.001) and O2Sat was lower (60 ± 11% vs 84 ± 1.6%, p = 0.002) at hospital admission than at discharge for the HAPE patients with follow-up ultrasound examinations. Regression analysis showed CTS was predictive of O2Sat (p < 0.001), and for every 1-point increase in CTS O2Sat fell by 0.67% (95% confidence interval, 0.41 to 0.93%, p < 0.001).

Conclusions: The comet-tail technique effectively recognizes and monitors the degree of pulmonary edema in HAPE. Reduction in CTS parallels improved oxygenation and clinical status in HAPE. The feasibility of this technique in remote locations and rapid correlation with changes in EVLW make it a valuable research tool.

Figures in this Article

High-altitude pulmonary edema (HAPE) is the leading cause of death from altitude illness.1Chest ultrasonography using the comet-tail technique has recently been shown to effectively detect pulmonary edema and quantify extravascular lung water (EVLW) in hospitalized patients. This technique relies on the creation of “comet-tail” artifacts by multiple microreflections of the ultrasound beam within water-thickened interlobular septa when pulmonary edema is present.26 This ultrasonographic technique, which is feasible in remote locations, can offer an important diagnostic aid in HAPE. As a research tool, it may also allow clarification of the time course of EVLW shifts in HAPE. We report on our clinical experience using the comet-tail technique in a remote, high-altitude setting, particularly for the diagnosis and monitoring of HAPE.

Patients and Clinical Treatment

From March 3, 2006, to May 20, 2006, 11 consecutive patients with a clinical diagnosis of HAPE were treated at the Himalayan Rescue Association clinic in Pheriche, Nepal (4,240 m). No patients seen at the clinic with a diagnosis of HAPE during that period were excluded from this report. The clinical diagnosis, which was based on the Lake Louise consensus definition of HAPE, was made prior to performing ultrasonography.7 All other patients who underwent chest ultrasonography using the comet-tail technique for clinical evaluation at the clinic during that time period (with the exception of one patient who had a clinical diagnosis of acute mountain sickness [AMS] and rales on chest examination) were used as control subjects. Admission vital signs were obtained at rest in a seated or near-supine (for patients unable to sit) position as soon after presentation as the patient could be situated in a chair or bed. Discharge vital signs were obtained at rest in the seated position for all patients. Oxygen saturation (O2Sat) was measured by finger pulse oximetry with patients breathing ambient air. Clinical features are described in Table 1 . By our institutional standards, this type of report does not require institutional review board approval or written informed consent from patients.

All 11 HAPE patients were treated with oxygen, nifedipine, and acetazolamide. Eight HAPE patients received additional sildenafil and salmeterol, and one patient received additional salmeterol only. The HAPE group included one patient who had been treated with all these agents, dexamethasone, and ceftriaxone for 12 h before presentation; the dexamethasone and ceftriaxone were discontinued on arrival. Two patients received treatment for concurrent diagnoses: one patient with high-altitude cerebral edema received dexamethasone, and one patient with gastroenteritis received ciprofloxacin. One patient required treatment in a portable hyperbaric chamber to conserve oxygen supplies. One patient descended from Pheriche immediately after presentation and treatment; the other 10 patients were admitted. One patient was evacuated by horse, and the patient with concurrent gastroenteritis was evacuated by helicopter. The remaining nine patients were able to walk out after discharge. We provided all patients with a 2-day supply of acetazolamide and nifedipine after discharge.

Ultrasound

Chest ultrasonography using the comet-tail technique was performed using accepted technique previously described in the literature.34 In brief, commercially available portable ultrasound equipment with a 2- to 4-MHz probe was ultilized (SonoSite 180PLUS; SonoSite; Bothell, WA).8 The ultrasonographic examinations were performed in the supine or near-supine positions. Ultrasound scanning of the anterior and lateral chest was performed in the midaxillary, anterior axillary, midclavicular, and parasternal positions of the second to fifth intercostal spaces on the right and the second to fourth intercostal spaces on the left for a total of 28 positions per complete examination. The comet-tail sign was defined as an echogenic, coherent, wedge-shaped signal with a narrow origin in the near field of the image, arising from the pleural line and extending to the edge of the screen (Fig 1 ). The sum of the number of comet-tail signs in all surveyed fields yielded the overall comet-tail score (CTS).

Seven of the 11 HAPE patients had repeat examinations at discharge from the clinic (mean time between examinations, 29 ± 16 h; range, 12 to 48 h), and 2 of those 7 patients had a third examination after returning to the area 1 week and 3 weeks after discharge, respectively. At the time of the third examination, both patients had clinical resolution of their HAPE. The ultrasonographer was aware of the clinical diagnosis in all 18 patients (27 examinations). A single ultrasound examination was performed on each subject at each time point, and a total CTS was assigned at that time by the ultrasonographer. All examination images were reread by the ultrasonographer in blinded fashion after the images were purged of identifying information and arbitrarily numbered and ordered. The images were similarly read twice in blinded fashion by a separate observer. These results were used to assess interobserver and intraobserver agreements.

Statistical Analysis

Descriptive statistics were used to demonstrate the overall frequencies with which comet-tails were identified in control patients, patients with HAPE, and in those HAPE patients in whom follow-up was available. Due to small study numbers and nonnormality of distribution as assessed by Shapiro-Wilks W testing, nonparametric techniques were used to compare unpaired (Kruskal-Wallis testing) and paired (Wilcoxon signed-rank testing) data.

To assess the proportion of change in O2Sat that was accounted for by number of comet-tails, linear regression analysis was employed. Multivariate modeling was used to assess whether the independent variables age or sex had significant impact on the dependent variable O2Sat.

To assess whether HAPE patients had comet-tails predominantly in a particular hemithorax at admission, the number of comet-tails per field in each hemithorax was calculated for each patient. A predominant side was designated when the number of comet-tails per field identified in one hemithorax was more than twice the number of comet-tails per field identified in the contralateral hemithorax.

For assessment of interrater consistency in assigning a comet-tail score, the κ method was utilized. The “absolute” κ option was employed to adjust for the fact that all possible integer values of the comet-tail score were not likely to be present in the observed data. Agreement was assessed for the total CTS. Given the 100% level of agreement ultimately identified between observers, the κ calculations were moot, but these data are still reported in the “Results” section.

All statistical calculations were performed using statistical software (STATA SE, version 9.2; StataCorp; College Station, TX). An α level of 0.05 was considered significant. Data are reported as mean ± SD.

Patients presenting with HAPE had higher CTS (31 ± 11 vs 0.86 ± 0.83) and lower O2Sat (61 ± 9.2% vs 87 ± 2.8%) than control subjects (p < 0.001 for both). CTS correlated with O2Sat (adjusted R2 = 0.62, p < 0.001). The distribution of CTS and O2Sat in all patients (HAPE and control) is described in Figure 2 .

CTS was significantly higher (35 ± 11 vs 12 ± 6.8, p = 0.002) and O2Sat was significantly lower (60 ± 11% vs 84 ± 1.6%, p < 0.001) at admission than at discharge for the seven HAPE patients with follow-up examinations. The maximum number of comet-tails identified in a single field in the HAPE patients was five. Changes in O2Sat and CTS at admission, discharge, and after clinical resolution of HAPE (where available) for the seven HAPE patients with follow-up studies are described in Figure 3 . Four of the 11 HAPE patients had a right-sided predominance to their comet-tails on admission, and 1 patient had a left-sided predominance.

Regression analysis showed CTS was predictive of O2Sat (p < 0.001). For every 1-point increase in CTS, O2Sat fell by 0.67% (95% confidence interval, 0.41 to 0.93%; p < 0.001). Changes in CTS accounted for 63.2% of the variability in O2Sat (by adjusted R2 calculation). Neither age (p = 0.86) nor sex (p = 0.93) were associated with change in O2Sat in univariate regression; when these covariates were forced into the model comprising CTS and O2Sat, there was no evidence of confounding or effect modification as assessed by point-estimate changes or interaction term significance.

κ analysis defining “agreement” as present when CTS readings were within two comet-tails found 100% interobserver agreement (SE for κ statistic 0.10, p < 0.0001). Intraobserver agreement was excellent: 91% for one observer, and 100% for the other (p < 0.0001 for both analyses). Notably, if “CTS agreement” was defined at a threshold of three comet-tails rather than two, a reasonable clinical standard, the intraobserver and interobserver agreements were both universal.

Our data demonstrate that ultrasound is an effective diagnostic and monitoring tool for HAPE. CTS correlated closely with clinical course, and with O2Sat. Others4 have alluded to the possible utility of the comet-tail technique for ongoing monitoring of pulmonary edema, but we are the first to report its routine clinical employment in this capacity for any disease process. This study marks the first time a nonradiologic measure of EVLW has been correlated with O2Sat in HAPE. The use of this novel technique to demonstrate a correlation between O2Sat and CTS, a qualitative measure of EVLW, buttresses a fundamental piece of pathophysiologic evidence regarding the role of edema in HAPE and supports the use of the technique in the study of HAPE.

We suggest that ultrasound may be superior to conventional radiography for diagnosis and monitoring of HAPE based on its merits, and because radiography is frequently unavailable in the remote locales where HAPE often occurs while ultrasound can be more easily transported to and maintained in such places. The quick responsiveness of CTS during the resolution of HAPE may recommend the comet-tail technique as superior to conventional radiography for monitoring HAPE patients, since chest radiographic abnormalities can lag behind clinical resolution in HAPE.911 While conventional radiology can identify pulmonary edema in many clinical scenarios including HAPE, it is frequently inaccurate for monitoring modest changes in EVLW and at high altitude may be slow to detect early pulmonary edema.1213 An appropriate ultrasound machine, which is significantly less expensive than a standard radiograph machine, has minimal operating costs. There are no contraindications to utilizing the technique and repeating examinations as frequently as desired. The technique is fast, easily learned, well tolerated by patients, does not employ ionizing radiation, and does not require a radiologist for interpretation.2 If an ultrasound machine with appropriate functionality is available and the operator is properly trained, the comet-tail technique can be combined with echocardiographic techniques for estimation of pulmonary artery pressure and left ventricular function to help differentiate between HAPE and left ventricular failure.

The demonstrated utility and feasibility of the comet-tail technique in a remote, high-altitude setting recommends it as a powerful research tool. We believe it is an ideal quantitative tool for physiologic and interventional investigations in HAPE. In a dedicated trial, this technique could describe, among other parameters, the natural history of EVLW shifts throughout both the onset and treatment of HAPE and could elucidate the part of various stimuli such as exercise in the initiation of EVLW accumulation in HAPE. It may also enable further investigation into the role of EVLW and subclinical pulmonary edema in normal high-altitude physiology and AMS. In many AMS sufferers and asymptomatic travelers to high altitude, rales on examination, impaired diffusing capacity, and altered pulmonary mechanics hypothesized to be due to subclinical pulmonary edema have been noted.1420 As alluded to earlier, conventional radiography has been shown to be particularly insensitive for detecting early HAPE and this type of subclinical pulmonary edema at high altitude.13,16 We are hopeful that the comet-tail technique will prove valuable where chest radiography falls short for these types of investigations.

The comet-tail technique is relatively new, and its use in HAPE, a unique form of noncardiogenic pulmonary edema, offers insights into the broader characteristics and utility of the technique. In the assessment of pulmonary edema, the comet-tail technique has heretofore been used to evaluate patient populations in which cardiogenic pulmonary edema predominates.3,6,21 Pulmonary artery wedge pressure (PAWP), which we did not measure in this study, is well known to be consistently normal or low in HAPE.9,2228 Our work implies that CTS does not in fact necessarily correlate with PAWP, as others have asserted.3 We think it likely that this described correlation was an artifact of studies3,21 conducted in populations in which cardiogenic pulmonary edema predominated. Ours is the first description of the comet-tail technique for the diagnosis of a noncardiogenic pulmonary edema, and it suggests that the technique will be generalizable to other forms of noncardiogenic pulmonary edema. Furthermore, our study findings call into question what criteria should be used in determining a “positive” chest ultrasound test finding for pulmonary edema. The most frequently employed definition in the literature requires multiple (defined as at least three comet-tail artifacts visible in a frozen image in one longitudinal scan with ≤ 7 mm between two of them) bilateral comet-tail images not confined laterally to the last intercostal spaces above the diaphragm.3,6 We had patients with as many as 40 comet-tails and > 1 comet-tail in multiple fields bilaterally who did not fulfill this widely employed definition of a positive test result, although such findings would seem to represent a significant degree of pulmonary edema. Admittedly, HAPE may be unique in this respect, due to the tendency for many patients to exhibit a unilateral predominance in the pattern of edema, thus reducing the frequency of multiple bilateral comet-tails as currently defined in the literature.11,26 For now, we do not recommend that the currently predominant standard for a positive test result be adopted for HAPE.

This study constitutes the first published report describing clinical experience with the use of chest ultrasonography for the evaluation of HAPE and attempts to highlight some the great potential we believe the technique holds for clinical and research purposes. Many of the limitations of the study derive from that fact that it was not a prospectively designed trial. We could not compare CTS to conventional chest radiography or PAWP, which were unavailable at the Himalayan Rescue Association clinic in Pheriche. Control subjects had to be derived from clinic patients with no suspicion for altitude illness, but who had clinically justifiable reasons to undergo chest ultrasonography. For this reason, our numbers are limited and our employment of the technique does not mirror its anticipated use in clinical practice in which patients with suspected HAPE would need to be differentiated from patients with other forms of altitude illness or pulmonary pathology. Some of the pulmonary pathologies that one might encounter in high-altitude populations, such as pneumonia or pulmonary fibrosis, can create comet-tails. With small numbers and few objective measures with which to compare our ultrasonographic results (O2Sat is the notable exception), we could not attempt to fully describe the clinical characteristics of the comet-tail technique for HAPE diagnosis such as sensitivity or specificity. Nevertheless, our data impact our understanding of the technique in general, its diagnostic role in HAPE, and the part of EVLW in HAPE. This study helps set the stage for the further use of chest ultrasonography for clinical and research purposes.

Abbreviations: AMS = acute mountain sickness; CTS = comet-tail score; EVLW = extravascular lung water; HAPE = high-altitude pulmonary edema; O2Sat = oxygen saturation; PAWP = pulmonary artery wedge pressure

This research was performed at the Himalayan Rescue Association Pheriche Clinic, Pheriche, Nepal.

No author received personal or financial support from, or has any affiliations or involvement with any organization with financial interest in the subject matter.

Table Graphic Jump Location
Table 1. Clinical Characteristics of HAPE and Control Patients at Presentation*
* 

Data are presented as No. of patients or mean ± SD unless otherwise indicated.

Figure Jump LinkFigure 1. Left, A: Ultrasound image of a control patient with no comet-tails. Right, B: Ultrasound image of comet-tails in a patient with HAPE.Grahic Jump Location
Figure Jump LinkFigure 2. Distribution of O2Sat and CTS in control and HAPE patients (adjusted R2 for CTS vs O2Sat = 0.62; p < 0.001). In order to provide a conservative, high-fidelity depiction of the relationship between CTS and O2Sat, we have provided a locally weighted scatterplot smoothing (lowess) graph generated by STATA SE 9.2 (StataCorp; College Station, TX) employing a standard lowess approach with running-line least-squares smoothing and incorporation of the Cleveland tricube weighting function. The bandwidth is 0.8, which is a standard setting that denotes that 0.8 × N observations used for calculating smoothed values for each point in the data (except for end points, for which smaller uncentered subsets are used).Grahic Jump Location
Figure Jump LinkFigure 3. Longitudinal changes in O2Sat and CTS over time in the seven HAPE patients with follow-up studies. Actual time from initial examination to each patient’s subsequent examination(s) was as follows: patient 1, –24 h, 7 days; patient 2, 48 h, 21 days; patient 3, 36 h; patient 4, 12 h; patient 5, 12 h; patient 6, 48 h; patient 7, 48 h.Grahic Jump Location
Hackett, PH, Roach, RC (2001) High altitude illness.N Engl J Med345,107-114. [PubMed] [CrossRef]
 
Picano, E, Frassi, F, Agricola, E, et al Ultrasound lung comets: a clinically useful sign of extravascular lung water.J Am Soc Echocardiogr2006;19,356-363. [PubMed]
 
Agricola, E, Bove, T, Oppizzi, M, et al “Ultrasound comet-tail images”: a marker of pulmonary edema: a comparative study with wedge pressure and extravascular lung water.Chest2005;127,1690-1695. [PubMed]
 
Jambrick, 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. [PubMed]
 
Lichtenstein, D, Meziere, G, Biderman, P, et al The comet-tail artifact: an ultrasound sign of alveolar-interstitial syndrome.Am J Respir Crit Care Med1997;158,1640-1646
 
Lichtenstein, D, Meziere, G A lung ultrasound allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact.Intensive Care Med1998;24,1331-1334. [PubMed]
 
The Lake Louise consensus on the definition and quantification of altitude illness. Sutton, J Coates, G Houston, C eds. Hypoxia and molecular medicine. 1993; Queen City Printers. Burlington, VT:.
 
Sonosite Corporation. Product specifications. Available at: http://www.sonosite.com/content/view/81/322/. Accessed July 1, 2006.
 
Hultgren, HN High altitude pulmonary edema. High altitude medicine. 1997; Hultgren Publications. Stanford, CA:.
 
Honigman, B, Yaron, M High altitude medicine. Marx, JA eds.Rosen’s emergency medicine: concepts and clinical practice2002,2044 Mosby. St. Louis, MO:
 
Vock, P, Brutsche, MH, Nanzer, A, et al Variable radiomorphologic data of high altitude pulmonary edema: features from 60 patients.Chest1991;100,1306-1311. [PubMed]
 
Halperin, BD, Feeley, TW, Mihm, FG, et al Evaluation of the portable chest roentgenogram for quantitating extravascular lung water in critically ill adults.Chest1985;88,649-652. [PubMed]
 
Vock, P, Fretz, C, Franciolli, M, et al High-altitude pulmonary edema: findings at high-altitude chest radiography and physical examination.Radiology1989;170,661-666. [PubMed]
 
Eldridge, MW, Braun, RK, Yoneda, KY, et al Effects of altitude and exercise on pulmonary capillary integrity: evidence for subclinical high-altitude pulmonary edema.J Appl Physiol2006;100,972-980. [PubMed]
 
Ge, RL, Matsuzawa, Y, Takeoka, M, et al Low pulmonary diffusing capacity in subjects with acute mountain sickness.Chest1997;111,58-64. [PubMed]
 
Cremona, G, Asnaghi, R, Baderna, P, et al Pulmonary extravascular fluid accumulation in recreational climbers: a prospective study.Lancet2002;359,303-309. [PubMed]
 
Hackett, P, Rennie, D The incidence, importance, and prophylaxis of acute mountain sickness.Lancet1976;2,1149-1155. [PubMed]
 
Singh, I, Khanna, PK, Srivastava, MC, et al Acute mountain sickness.N Engl J Med1969;280,175-184. [PubMed]
 
Raymond, LW Altitude pulmonary edema below 8,000 feet: what are we missing?Chest2003;123,5-7. [PubMed]
 
Mason, NP, Petersen, M, Melot, C, et al Serial changes in nasal potential difference and lung electrical impedance tomography at high altitude.J Appl Physiol2003;94,2043-2050. [PubMed]
 
Agricola, E, Picano, E, Oppizzi, M, et al Assessment of stress-induced pulmonary interstitial edema by chest ultrasound during exercise echocardiography and its correlation with left ventricular function.J Am Soc Echocardiogr2006;19,457-463. [PubMed]
 
Kubo, K, Hanaoka, M, Hayano, T, et al Inflammatory cytokines in BAL fluid and pulmonary hemodynamics in high-altitude pulmonary edema.Respir Physiol1998;111,301-310. [PubMed]
 
Koizumi, T, Kawashima, A, Kubo, K, et al Radiographic and hemodynamic changes during recovery from high-altitude pulmonary edema.Intern Med1994;33,525-528. [PubMed]
 
Maggiorini, M, Melot, C, Pierre, S, et al High-altitude pulmonary edema is initially caused by an increase in capillary pressure.Circulation2001;103,2078-2083. [PubMed]
 
Hultgren, HN, Lopez, CE, Lundberg, E, et al Physiologic studies of pulmonary edema at high altitude.Circulation1964;29,393-408. [PubMed]
 
Kobayashi, T, Koyama, S, Kubo, K, et al Clinical features of patients with high-altitude pulmonary edema in Japan.Chest1987;92,814-821. [PubMed]
 
Roy, SB, Guleria, JS, Khanna, PK, et al Haemodynamic studies in high altitude pulmonary oedema.Br Heart J1969;31,52-58. [PubMed]
 
Penaloza, D, Sime, F Circulatory dynamics during high altitude pulmonary edema.Am J Cardiol1969;23,369-378. [PubMed]
 

Figures

Figure Jump LinkFigure 1. Left, A: Ultrasound image of a control patient with no comet-tails. Right, B: Ultrasound image of comet-tails in a patient with HAPE.Grahic Jump Location
Figure Jump LinkFigure 2. Distribution of O2Sat and CTS in control and HAPE patients (adjusted R2 for CTS vs O2Sat = 0.62; p < 0.001). In order to provide a conservative, high-fidelity depiction of the relationship between CTS and O2Sat, we have provided a locally weighted scatterplot smoothing (lowess) graph generated by STATA SE 9.2 (StataCorp; College Station, TX) employing a standard lowess approach with running-line least-squares smoothing and incorporation of the Cleveland tricube weighting function. The bandwidth is 0.8, which is a standard setting that denotes that 0.8 × N observations used for calculating smoothed values for each point in the data (except for end points, for which smaller uncentered subsets are used).Grahic Jump Location
Figure Jump LinkFigure 3. Longitudinal changes in O2Sat and CTS over time in the seven HAPE patients with follow-up studies. Actual time from initial examination to each patient’s subsequent examination(s) was as follows: patient 1, –24 h, 7 days; patient 2, 48 h, 21 days; patient 3, 36 h; patient 4, 12 h; patient 5, 12 h; patient 6, 48 h; patient 7, 48 h.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Clinical Characteristics of HAPE and Control Patients at Presentation*
* 

Data are presented as No. of patients or mean ± SD unless otherwise indicated.

References

Hackett, PH, Roach, RC (2001) High altitude illness.N Engl J Med345,107-114. [PubMed] [CrossRef]
 
Picano, E, Frassi, F, Agricola, E, et al Ultrasound lung comets: a clinically useful sign of extravascular lung water.J Am Soc Echocardiogr2006;19,356-363. [PubMed]
 
Agricola, E, Bove, T, Oppizzi, M, et al “Ultrasound comet-tail images”: a marker of pulmonary edema: a comparative study with wedge pressure and extravascular lung water.Chest2005;127,1690-1695. [PubMed]
 
Jambrick, 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. [PubMed]
 
Lichtenstein, D, Meziere, G, Biderman, P, et al The comet-tail artifact: an ultrasound sign of alveolar-interstitial syndrome.Am J Respir Crit Care Med1997;158,1640-1646
 
Lichtenstein, D, Meziere, G A lung ultrasound allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact.Intensive Care Med1998;24,1331-1334. [PubMed]
 
The Lake Louise consensus on the definition and quantification of altitude illness. Sutton, J Coates, G Houston, C eds. Hypoxia and molecular medicine. 1993; Queen City Printers. Burlington, VT:.
 
Sonosite Corporation. Product specifications. Available at: http://www.sonosite.com/content/view/81/322/. Accessed July 1, 2006.
 
Hultgren, HN High altitude pulmonary edema. High altitude medicine. 1997; Hultgren Publications. Stanford, CA:.
 
Honigman, B, Yaron, M High altitude medicine. Marx, JA eds.Rosen’s emergency medicine: concepts and clinical practice2002,2044 Mosby. St. Louis, MO:
 
Vock, P, Brutsche, MH, Nanzer, A, et al Variable radiomorphologic data of high altitude pulmonary edema: features from 60 patients.Chest1991;100,1306-1311. [PubMed]
 
Halperin, BD, Feeley, TW, Mihm, FG, et al Evaluation of the portable chest roentgenogram for quantitating extravascular lung water in critically ill adults.Chest1985;88,649-652. [PubMed]
 
Vock, P, Fretz, C, Franciolli, M, et al High-altitude pulmonary edema: findings at high-altitude chest radiography and physical examination.Radiology1989;170,661-666. [PubMed]
 
Eldridge, MW, Braun, RK, Yoneda, KY, et al Effects of altitude and exercise on pulmonary capillary integrity: evidence for subclinical high-altitude pulmonary edema.J Appl Physiol2006;100,972-980. [PubMed]
 
Ge, RL, Matsuzawa, Y, Takeoka, M, et al Low pulmonary diffusing capacity in subjects with acute mountain sickness.Chest1997;111,58-64. [PubMed]
 
Cremona, G, Asnaghi, R, Baderna, P, et al Pulmonary extravascular fluid accumulation in recreational climbers: a prospective study.Lancet2002;359,303-309. [PubMed]
 
Hackett, P, Rennie, D The incidence, importance, and prophylaxis of acute mountain sickness.Lancet1976;2,1149-1155. [PubMed]
 
Singh, I, Khanna, PK, Srivastava, MC, et al Acute mountain sickness.N Engl J Med1969;280,175-184. [PubMed]
 
Raymond, LW Altitude pulmonary edema below 8,000 feet: what are we missing?Chest2003;123,5-7. [PubMed]
 
Mason, NP, Petersen, M, Melot, C, et al Serial changes in nasal potential difference and lung electrical impedance tomography at high altitude.J Appl Physiol2003;94,2043-2050. [PubMed]
 
Agricola, E, Picano, E, Oppizzi, M, et al Assessment of stress-induced pulmonary interstitial edema by chest ultrasound during exercise echocardiography and its correlation with left ventricular function.J Am Soc Echocardiogr2006;19,457-463. [PubMed]
 
Kubo, K, Hanaoka, M, Hayano, T, et al Inflammatory cytokines in BAL fluid and pulmonary hemodynamics in high-altitude pulmonary edema.Respir Physiol1998;111,301-310. [PubMed]
 
Koizumi, T, Kawashima, A, Kubo, K, et al Radiographic and hemodynamic changes during recovery from high-altitude pulmonary edema.Intern Med1994;33,525-528. [PubMed]
 
Maggiorini, M, Melot, C, Pierre, S, et al High-altitude pulmonary edema is initially caused by an increase in capillary pressure.Circulation2001;103,2078-2083. [PubMed]
 
Hultgren, HN, Lopez, CE, Lundberg, E, et al Physiologic studies of pulmonary edema at high altitude.Circulation1964;29,393-408. [PubMed]
 
Kobayashi, T, Koyama, S, Kubo, K, et al Clinical features of patients with high-altitude pulmonary edema in Japan.Chest1987;92,814-821. [PubMed]
 
Roy, SB, Guleria, JS, Khanna, PK, et al Haemodynamic studies in high altitude pulmonary oedema.Br Heart J1969;31,52-58. [PubMed]
 
Penaloza, D, Sime, F Circulatory dynamics during high altitude pulmonary edema.Am J Cardiol1969;23,369-378. [PubMed]
 
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