Key words
pleural effusion - sonography - volumetric assessment - chest CT
Introduction
Chest sonography is a viable bedside method to verify free fluid and to differentiate
contained effusions, pleural peel, atelectasis, diaphragmatic elevation, and other
lesions [1]
[2]
[3]
[4]
[5]. To date, there is no reliable method for the fast quantification of pleural effusions
in intensive care unit (ICU) patients as a diagnostic basis for puncture or drainage.
In 1994, Eibenberger et al. developed a sonographic method for the volumetric quantification
of pleural effusions in a strictly supine position [6]. In this study, the extent of the effusion was measured sonographically in each
intercostal space. From these measurements and the effusion volumes, which were quantified
by puncture, a formula was developed to estimate effusion volumes.
Such methods are feasible in ICU patients because they are rarely able to sit upright
[6]
[7]. This is especially true for consciously sedated and ventilated patients. Patients
in respiratory distress who are not intubated and often ventilated suffer from orthopnea
and are unable to lie flat on their back. Schmidt et al. developed a method for the
estimation of pleural effusion volumes in patients with a 30° inclination of the torso
[8]. The pleural effusion volume was defined as the sum of the basal expanse of the
free fluid between the diaphragm, the inferior lobe of the lung, and the maximum craniocaudal
expanse of the effusion multiplied by a factor of 70. This method is adequate and
feasible for ICU patients with a slight inclination of the torso. However, this approach
requires multiple measurements and is therefore relatively time-consuming and less
feasible in an ICU setting.
The aim of this prospective non-randomized study was to develop a simple and fast
method for the bedside sonographic quantification of pleural effusions in ICU patients.
Materials and Methods
Patient cohort
Overall, 22 patients (median age: 58.5 years, range: 37–88 years, 14 male and 8 female
patients) with a total of 31 pleural effusions were sonographically examined in a
university hospital. A chest CT was performed on all patients as part of the clinical
and diagnostic routine prior to the ultrasound exam. All CT scans were then assessed
and evaluated by an experienced radiologist. If pleural effusions were detected, the
patient was re-examined with an additional sonogram. The inclusion criteria demanded
that the chest CT and the ultrasound exam be performed less than six hours apart and
that the patient had not yet been treated with effusion puncture or drainage prior
to the ultrasound exam. Finally, only patients with uncontained effusions were included
in this study.
Sonographic measurements of pleural effusion
The sonographic exam was performed while the patient’s torso was positioned at a 30°
incline. Intercostal spaces (ICSs) 4-9 were traced in the posterior axillary line
(PAL) with a 3.5-MHz curved linear transducer head of an ultrasound unit type EUB
405 (Hitachi Medical Systems, Tokyo, Japan). The ICSs were identified on the basis
of anatomical landmarks such as the claviculae and vertebral bodies and used as acoustic
windows. The transducer head was tilted until the effusion became visible on the ultrasound
screen. The expanse of the fluid moat between the visceral pleura and the parietal
pleura was measured in millimeters. The most caudal portion of the effusion was chosen
for each measurement ([Fig. 1]).
Fig. 1 Measurement of the liquid crescent of the pleural effusion during sonography.
Computed tomographic volumetry
The patients were selected on the basis of routine diagnostic CT scans, which depicted
the entire pleural effusion. All scans were performed on a 4-slice spiral CT scanner
with a slice thickness of 5 mm and a pitch of 2. The pleural effusion volume was calculated
using semi-automated volumetric software with threshold analysis and contour limiting
on an Easyvison workstation (Philips Healthcare, Best, the Netherlands). A threshold
analysis was used to subtract the air and skeletal structures from the calculated
volume. Each image slice was examined and evaluated individually. The area of effusion
was delineated with the cursor in each image slice by the radiologist ([Fig. 2]). The computer program then calculated the total volume of the pleural effusion
from the sum of each demarcated region and slice thickness.
Fig. 2 CT reconstruction in 3 planes: Region marked with cursor (green: volume considered
in total volume calculation) in a single CT image slice after threshold analysis (red:
volume not considered for total volume calculation).
Statistical analysis
The sonographically measured values in millimeters were compared to the CT-calculated
volumes in a scatter plot. The CT volumes and the maximum extent of the effusion were
compared using linear regression analysis. The regression line equations were then
used to calculate the pleural effusion volumes, which were then compared to the corresponding
CT-calculated volumes. An interclass correlation coefficient (ICC) was determined
for each comparison. On the basis of the regression line function of the ICS with
the highest ICC and the smallest two-way confidence interval (CI), a formula was developed
to calculate the pleural effusion volumes with the sonographic image data.
Results
To assess and measure the maximum interpleural expanse of the effusions, a sonographic
window at the sixth ICS in the PAL is ideal. Both the CI and ICC for the sixth ICS
as sonographic windows confirm this hypothesis in [Fig. 3].
Fig. 3 Regression diagram for the 6th ICS: measured volume (CT data) over thickness of liquid
head in the 6th ICS (ultrasound data).
The sixth ICS regression line equation is as follows:
VolumeCT (ml) = 13.330 × sectionultrasound (mm) + 27.134
The regression coefficient for the regression line of the sixth ICS was r=0.767. The
coefficient of determination was R2=0.589 with a 95% CI of 9.017-17.643 of the regression line. The ICC for the sixth
ICS was 0.7487 (p<0.00001; 95% CI 0.5393-0.8714).
Because the absolute coefficient loses its mathematical relevance in practice, the
absolute coefficient is negligible in favor of a simplified formula:
veffusion in CT (ml) = 13.330 × thicknessliquid head in the sixth ICS (mm)
We have listed the rounded values with which the estimation of the pleural effusion
volume is more comfortable and considered the standard deviation in [Table 1].
Table 1 Estimation of effusion volume with sonographically measured liquid crescent.
|
Thickness of liquid crescent in sonography (mm)
|
Estimated volume of the effusion (ml)
|
Standard deviation (ml)
|
|
5
|
70
|
20
|
|
10
|
130
|
40
|
|
15
|
200
|
60
|
|
20
|
270
|
90
|
|
30
|
400
|
130
|
|
40
|
530
|
170
|
|
50
|
670
|
220
|
|
60
|
800
|
260
|
|
70
|
930
|
300
|
|
80
|
1070
|
350
|
|
90
|
1200
|
390
|
|
100
|
1330
|
430
|
Discussion
In the verification of pleural effusions, sonography (sensitivity: 100%, specificity:
99.7%) is superior to chest X-ray in an erect patient (sensitivity: 71%, specificity:
98.5%) [1]
[9]. Moreover, an upright chest X-ray is impossible for most ICU patients with severe
primary diseases and impaired physical stamina. The sonographic identification of
pleural effusions is simple; the effusions appear echo-free, are sharply delineated,
and show dorsal echo enhancement [2]
[3]. Since atelectasis, diaphragmatic elevation, tumors, and pleural sheaths cause no
difficulty with respect to differentiation on ultrasound images as in conventional
fluoroscopic images, larger effusions can be diagnosed effortlessly [1]
[2]
[5]. An effusion volume of at least 150 ml is necessary for the diagnosis of an uncontained
pleural effusion on a standard X-ray in an erect patient [10]. However, 5-ml effusion volumes in the basal and laterodorsal compartment between
the ribcage and the diaphragm suffice for a reliable sonographic diagnosis [10]. The ultrasound examination can be performed bedside and can be repeated easily
and quickly for control purposes. Compared to conventional chest X-ray, sonography
is the more precise method and is also readily available in most ICUs [6].
In this study, a sonogram was performed on patients whose torso was inclined by 30°.
The image data were collected during expiration. In 1994, Eibenberger et al. examined
51 patients with pleural effusions in a strictly supine position at maximum inspiration.
In this study, the expanse of the pleural effusion was measured sonographically. Measurements
were taken between the parietal and visceral pleura. In the second step, the effusion
was punctured in 200-ml increments until the entire effusion was drained. Sonographic
measurements were taken between each puncture from the same angle. All 331 sonographic
measurements were then compared to the drained volumes using regression analysis.
Statistical analysis rendered the following formula: y=47.6×– 837 (the formula proposed
in this paper is V=13.330 x ICR6) with y equaling the approximated effusion volume
(ml) and x being the maximum expanse of the effusion (mm). The arithmetic median standard
deviation was +/− 224 ml [6].
In a further study, Balik et al. examined 81 patients with pleural effusions in a
supine position with a torso elevation of 15°. The maximum separation between the
parietal and visceral pleura (Sep) at maximum expiration was measured. Thoracocentesis
was performed and the total volume of the drained effusion was determined. The pleural
effusion was calculated as follows: V (ml)=20 * Sep (mm). The mean predictive error
of V in this method was 158 ml ± 160.6 ml [11]. For comparison, in our study, the arithmetic median standard deviation was slightly
worse at +/− 204.85 ml.
However, these values should be seen in a clinical context. An exact quantification,
i. e., 260 ml exactly, is most likely less important than the ability to determine
if an effusion volume is in the range of 200 ml or 300 ml.
Ventilated lateral lung compartments may mask small effusions and thus impede reliable
measurement of the effusion, especially during deep inspiration [12]. Therefore, sonographic measurements were performed during expiration. The patients
were asked to breathe calmly and normally, with the goal of achieving comparability
between spontaneous breathing and ventilated patients.
In this study, CT volumetry was used as a reference volume (the gold standard). We
based this decision on studies that showed good correlation between the actual organ
volumes and CT-calculated volumes [13]
[14]
[15]
[16]
[17]. It needs to be further evaluated whether CT calculations render more precise results
than drainage in the quantification of effusion volumes. After the puncture of a pleural
effusion, a residual volume may remain within the interpleural space and could thus
lead to an underestimation of the total effusion volume. With CT volumetry, the entire
effusion volume is imaged. However, this method can lead to other sources of error,
such as the breath-induced movement of the thoracic organs. Since all CT scans were
performed in a spiral CT, the patients were asked to hold their breath for 20 to 40 s.
The scan technique errors caused by breath-induced movements are negligible [18]. Moreover, outlining the effusion with the cursor in each image slice can induce
user-related errors [18]. Through the predefinition of a density threshold in CT excluding air and bone from
the soft tissue image, merely intercostal musculature and atelectasis had to be differentiated
from the effusion. The intercostal musculature was easy to differentiate due to its
anatomic location; atelectases were precluded from the volume due to differences in
density on the CT images. Differentiation from the diaphragm and liver in the abdominal
slices of the CT images was also achieved using the anatomic location and density.
Drainage of pleural effusions for the diagnostic determination of effusion volume
is an invasive method that leads to risks such as bleeding, infection, and pneumothorax.
The formula we describe herein for the estimation of pleural effusion volumes with
sonography is a dimension-free function describing a regression line. This allows
the estimation of an effusion volume from a sonographically measured distance, i. e.,
the maximum expanse of the effusion measured from the sixth ICS. Further validation
of the formula with a larger patient cohort and differentiation between ventilated
and spontaneously breathing patients are necessary. To ensure simplicity and clinical
feasibility, we assembled rounded measurements of the maximum expanse of the effusion
to simplify the clinical quantification ([Table 1]).
This technique can be used for bedside examinations in most clinical settings due
to the wide availability and mobility of modern ultrasound units [19]
[20]. Sonography of pleural effusions is a feasible method for critically ill patients
who are mechanically ventilated [11]
[21]
[22]. Moreover, a sonographic examination does not expose the patient or physician to
ionizing radiation [19]. The ultrasound volumetric estimation of pleural effusions permits both determination
of an indication for drainage and determination of the ideal puncture point [6]
[8]
[23]
[24]. Furthermore, sonography is a cost-efficient method [19].
Our results are comparable to those noted in the cited studies, which used drainage
as the gold standard for quantification. In contrast to the existing literature, we
took advantage of the accuracy of CT volumetry and avoided the disadvantages and inaccuracies
of drainage.
In conclusion, the ultrasound volumetric estimation of pleural effusion volumes is
easy, cost-efficient, and clinically feasible using the proposed method. This method
is ideal in critically ill ICU patients for bedside determination of an indication
for pleural effusion diagnostics and drainage.
