Chest Ultrasonography for the Diagnosis and

Monitoring of High-Altitude Pulmonary

Edema*
Peter J. Fagenholz, Jonathan A. Gutman, Alice F. Murray, Vicki E.
Noble, Stephen H. Thomas and N. Stuart Harris

Chest 2007;131;1013-1018
DOI 10.1378/chest.06-1864
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by the American College of Chest Physicians, 3300 Dundee Road,
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 CHEST Original Research
CHEST IMAGING

Chest Ultrasonography for the

Diagnosis and Monitoring of High-
Altitude Pulmonary Edema*
Peter J. Fagenholz, MD; Jonathan A. Gutman, MD; Alice F. Murray, MBChB;
Vicki E. Noble, MD; Stephen H. Thomas, MD, MPH; and
N. Stuart Harris, MD, MFA

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 extravas-
cular 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 ⴞ SD, 31 ⴞ 11 vs 0.86 ⴞ 0.83]
and lower oxygen saturation (O2Sat) [61 ⴞ 9.2% vs 87 ⴞ 2.8%] than control subjects (p < 0.001
for both). Mean CTS was higher (35 ⴞ 11 vs 12 ⴞ 6.8, p < 0.001) and O2Sat was lower (60 ⴞ 11%
vs 84 ⴞ 1.6%, p ⴝ 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. (CHEST 2007; 131:1013–1018)

Key words: acute mountain sickness; high-altitude pulmonary edema; hypoxia; mountaineering; pulmonary edema;
ultrasound

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

H igh-altitude pulmonary edema (HAPE) is the

leading cause of death from altitude illness. 1
Chest ultrasonography using the comet-tail tech-
*From the Departments of Surgery (Dr. Fagenholz) and Emer-
gency 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.
This research was performed at the Himalayan Rescue Associa-
tion 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.
nique has recently been shown to effectively detect
pulmonary edema and quantify extravascular lung
water (EVLW) in hospitalized patients. This tech-
nique relies on the creation of “comet-tail” artifacts
Manuscript received July 31, 2006; revision accepted October 8,
2006.
Reproduction of this article is prohibited without written permission
from the American College of Chest Physicians (www.chestjournal.
org/misc/reprints.shtml).
Correspondence to: N. Stuart Harris, MD, MFA, Department of
Emergency Medicine, Clinics 115, Massachusetts General Hospi-
tal, 55 Fruit St, Boston, MA 02140; e-mail: nsharris@partners.org
DOI: 10.1378/chest.06-1864

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© 2007 American College of Chest Physicians
by multiple microreflections of the ultrasound beam
within water-thickened interlobular septa when pul-
monary edema is present.2– 6 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
For editorial comment see page 951
time course of EVLW shifts in HAPE. We report on
our clinical experience using the comet-tail tech-
nique in a remote, high-altitude setting, particularly
for the diagnosis and monitoring of HAPE.
Materials and Methods
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 in-
formed 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 ceftriax-
one for 12 h before presentation; the dexamethasone and ceftri-
axone were discontinued on arrival. Two patients received treat-
ment for concurrent diagnoses: one patient with high-altitude
cerebral edema received dexamethasone, and one patient with

Table 1—Clinical Characteristics of HAPE and Control Patients at Presentation*

Characteristics HAPE Control

Total patients 11 7
Age, yr
Mean 34 ⫾ 12 34 ⫾ 9.1
Range 21–54 22–50
Male/female gender 9/2 5/2
National origin
Nepal 7 (includes 2 Sherpa) 3 (includes 1 Sherpa)
Other 1 each for Japan, United States, Canada, and Poland 2 for Unites States; 1 each for Germany and
Australia
Medical history Chronic musculoskeletal pain (n ⫽ 1); regular alcohol Hypertension (n ⫽ 1)
use (three drinks/d)关n ⫽ 1兴; tobacco use (three
cigarettes/wk)[n ⫽ 1]

History of altitude illness AMS (n ⫽ 2); headache (n ⫽ 1) None

Heart rate, beats/min 121 ⫾ 20 77 ⫾ 6.5
Range 77–150 72–88
Respiratory rate, breaths/min 35 ⫾ 8.3 12 ⫾ 2.1
Range 20–50 8–14
O2Sat, % 61 ⫾ 9.2 87 ⫾ 2.8
Rales
Bilateral, all fields 4 0
Bilateral, localized 4 0
Unilateral 3 0
Cyanosis
Central 2 0
Peripheral 3 0
None 6 7
Maximum altitude, m
⬎ 5,000 4 2
4,500–5,000 7 1
⬍ 4,500 0 4
Concurrent diagnosis Gastroenteritis (n ⫽ 1); high-altitude cerebral Nocturnal periodic breathing (n ⫽ 2); high-altitude
edema (n ⫽ 1) cough (n ⫽ 2); bruised rib (n ⫽ 1)
*Data are presented as No. of patients or mean ⫾ SD unless otherwise indicated.

1014 Original Research

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© 2007 American College of Chest Physicians
gastroenteritis received ciprofloxacin. One patient required treat-
ment 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.3,4 In brief, commercially available portable ultrasound
equipment with a 2- to 4-MHz probe was ultilized (SonoSite
180PLUS; SonoSite; Bothell, WA).8 The ultrasonographic exam-
inations were performed in the supine or near-supine positions.
Ultrasound scanning of the anterior and lateral chest was per-
formed 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 ultrasonog-
rapher 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
Figure 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.
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© 2007 American College of Chest Physicians
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 un-
paired (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 predomi-
nantly 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 ␬ method was utilized. The “absolute” ␬ 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 ␬
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 ␣ level of 0.05 was considered significant. Data are
reported as mean ⫾ SD.
Results
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
CHEST / 131 / 4 / APRIL, 2007 1015

Figure 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).
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 pa-
tients 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
Figure 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 examina-
tion(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.
1016
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© 2007 American College of Chest Physicians
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 ac-
counted 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.
␬ analysis defining “agreement” as present when
CTS readings were within two comet-tails found
100% interobserver agreement (SE for ␬ statistic
0.10, p ⬍ 0.0001). Intraobserver agreement was ex-
cellent: 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 agree-
ments were both universal.
Discussion
Our data demonstrate that ultrasound is an effec-
tive 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 corre-
lated 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 monitor-
ing 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 radiogra-
phy for monitoring HAPE patients, since chest
radiographic abnormalities can lag behind clinical
resolution in HAPE.9 –11 While conventional radiol-
ogy can identify pulmonary edema in many clinical
scenarios including HAPE, it is frequently inaccurate
for monitoring modest changes in EVLW and at high
Original Research
altitude may be slow to detect early pulmonary
edema.12,13 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 tech-
nique and repeating examinations as frequently as
desired. The technique is fast, easily learned, well
tolerated by patients, does not employ ionizing radi-
ation, and does not require a radiologist for interpre-
tation.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 func-
tion to help differentiate between HAPE and left
ventricular failure.
The demonstrated utility and feasibility of the
comet-tail technique in a remote, high-altitude set-
ting 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.14 –20 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 radiogra-
phy 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.9,22–28 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
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© 2007 American College of Chest Physicians
comet-tail technique for the diagnosis of a noncar-
diogenic 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 ⱕ 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 gen-
eral, its diagnostic role in HAPE, and the part of
CHEST / 131 / 4 / APRIL, 2007 1017
EVLW in HAPE. This study helps set the stage for
the further use of chest ultrasonography for clinical
and research purposes.
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Original Research
 Chest Ultrasonography for the Diagnosis and Monitoring of
High-Altitude Pulmonary Edema *
Peter J. Fagenholz, Jonathan A. Gutman, Alice F. Murray, Vicki E. Noble,
Stephen H. Thomas and N. Stuart Harris
Chest 2007;131; 1013-1018
DOI 10.1378/chest.06-1864
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© 2007 American College of Chest Physicians