REVIEW

CURRENT
OPINION Lung volume assessment in acute respiratory
distress syndrome
Lu Chen and Laurent Brochard

Purpose of review
Measurements of lung volumes allow evaluating the pathophysiogical severity of acute respiratory distress
syndrome (ARDS) in terms of the degree of reduction in aerated lung volume, calculating strain, quantifying
recruitment and/or hyperinflation, and gas volume distribution. We summarize the current techniques for
lung volume assessment selected according to their possible usage in the ICU and discuss the recent
findings obtained with implementation of these techniques in patients with ARDS.
Recent findings
Computed tomography technique remains irreplaceable in terms of quantitative aeration of different lung
regions, but the commonly used cut-offs for classification may be questioned with recent findings on
nonpathological lungs. Monitoring end expiratory lung volume using nitrogen washout technique enhanced
our understanding on lung volume change during positioning, pleural effusion drainage, intra-abdominal
hypertension, and recruitment maneuver. Recent studies supported that tidal volume could not surrogate
tidal strain, which needs measurement of functional residual capacity and which is correlated with pro-
inflammatory lung response.
Summary
Although lung volume measurements are still limited to research area of ARDS, recent progress in
technology provides clinicians more opportunities to evaluate lung volumes noninvasively at the bedside
and may facilitate individualization of ventilator settings based on the specific physiological understandings
of a given patient.
Keywords
acute lung injury, functional residual capacity, lung volume, strain, stress

INTRODUCTION ‘volutrauma’ [4]. Because of the reduction of aerated

Acute respiratory distress syndrome (ARDS) is
characterized by various degrees of reduction in
aerated lung volume due to alveolar flooding, con-
solidation, and atelectasis. Since the earlier research
in ARDS, the relationship between defects in
oxygenation, impairment in mechanics, and lung
volume loss was evidenced [1,2]. Measurements of
lung volumes can be an obvious way to scale the
severity of ARDS, but it took a long time before the
different techniques could be used at bedside in
clinical practice.
Volutrauma and the concept of strain
Dreyfuss et al. [3] found that high tidal volume,
generated either by positive intra-thoracic pressure
or negative extra-thoracic pressure, was a major
contributor in ventilator-induced pulmonary
edema, leading them to propose the term
lung volume in ARDS, the need to ventilate the
lungs with lower tidal volume (Vt) than convention-
al setting (10–15 ml/kg) or even than normal indivi-
duals (7–8 ml/kg), was proposed to reduce
volutrauma. This was subsequently proven
beneficial by the ARDSnet landmark clinical trial
[5], and a target Vt of 6 ml/kg of predicted body
weight (PBW) has been widely used in ARDS. How-
ever, it is still controversial to know whether 6 ml/kg
PBW – an arbitrary cut-off – is the optimum setting
Interdepartmental Division of Critical Care Medicine, University of
Toronto, Keenan Research Institute, and Department of Critical Care
Medicine, St Michael’s Hospital, Toronto, Ontario, Canada
Correspondence to Laurent Brochard, Department of Critical Care
Medicine, St Michael’s Hospital, 30 Bond Street, Toronto, ON M5B
1W8, Canada. Tel: +1 416 864 5686; e-mail: BrochardL@smh.ca
Curr Opin Crit Care 2015, 21:259–264
DOI:10.1097/MCC.0000000000000193

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Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

Cardiopulmonary monitoring
KEY POINTS

Lung volume measurements represent a strong potential
clinical interest for individualization of ventilator settings
to reduce the risks of ventilator-induced lung injury in
patients with ARDS.

Quantitative measurements of static lung volumes can
provide valuable information and have become easier
to use in clinical practice.

Data indicate that the reliability of lung volume
measurements may depend on ventilatory settings.

Electrical impedance tomography has been
increasingly investigated as a new tool to
semiquantitatively assess dynamic changes in lung
volumes at the bedside.
for all patients with ARDS. Recent studies indicated
that the risk of Vt-induced overdistension or volu-
trauma depends on the amount of aerated tissue
receiving the gas. A term from the field of contin-
uum mechanics – strain – has been used to describe
the lung deformation related to its original status:
Vt-induced strain is the ratio of Vt to functional
residual capacity (FRC). Consequently, the same
Vt/PBW may generate much greater strain in case
of low FRC than with high FRC; 6 ml/kg still may be
excessive in a patient with extremely reduced FRC
and may be unnecessarily low in a patient with a
well preserved FRC, at the price of deep sedation or
paralysis. Therefore, individualized setting of Vt
based on strain seems physiologically sound and
of potential benefit. This approach requires a valid
measurement of FRC.
Positive end-expiratory pressure and
recruitment
Positive end-expiratory pressure (PEEP) has been
applied in patients with ARDS for the purpose of
recruiting collapsed lung tissue, or more exactly for
keeping open the recruited lung. The main con-
sequence of PEEP is the increase in end-expiratory
lung volume (EELV), which consists of two parts:
recruitment of previously non/poorly aerated
tissue, and inflation or hyperinflation of previously
normally aerated tissue. For example, in a highly
recruitable patient, a large amount of the increase
in EELV is caused by reopening of previously
collapsed lung tissue, whereas in a poorly recruitable
patient, the increase in EELV is generated by
inflation of previously open lung tissue which
may lead to hyperinflation. Therefore, the effec-
tiveness of PEEP depends on assessment of recruit-
ability.
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Limited use in clinical practice
Despite its strong potential clinical interest, assess-
ment of lung volume at the bedside is limited due to
the complexities of the techniques used in the past.
Recent progress in technology may facilitate the
application of either absolute lung volume measure-
ments or changes in lung volume. We will summar-
ize the current techniques available for lung volume
assessment in the ICU and the recent findings
obtained with implementation of these techniques
in patients with ARDS.
ABSOLUTE LUNG VOLUMES
Three types of techniques are available for measur-
ing the absolute or static lung volumes in patients
with ARDS.
Gas dilution technique
Gas dilution technique has been applied to measure
static lung volumes for more than two centuries. It is
based on equilibration of gas in the lung with a
known volume of gas containing a known fraction
of an inert gas. The multibreath helium equili-
bration technique has been used as a common
method for measuring FRC in pulmonary function
test laboratory, but was essentially used for clinical
research in mechanically ventilated patients due to
technical complexity. Pesenti’s group proposed a
simplified helium dilution method in terms of
instrumentation. They concluded that this simpli-
fied helium dilution method is clinically acceptable
when applied in ventilated patients with a short
time constant of the respiratory system, such as
ARDS patients [6,7]. A dilution technique using
methane is also possible [8], but neither these sim-
plified techniques nor the classical helium dilution
technique can be performed without disconnection
from the ventilator or without the use of relatively
cumbersome equipment. Because of its complexity,
gas dilution technique is still limited to research
purpose in ARDS.
Computed tomography scan technique
Quantitative analysis of computed tomography
(CT) scans enables an accurate evaluation of the
volume of gas and tissue in the lungs of ARDS
patients. It is based on the linear correlation
between the X-ray attenuation in a given volume
and the physical density of that volume, namely,
the radiodensity. The Hounsfield unit scale (HU) or
CT numbers is a quantitative scale for describing
radiodensity. It refers to a dimensionless index of
X-ray attenuation that is related to the attenuation
of air and water, with an arbitrary allocation of the
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radiodensity of distilled water to 0 HU, whereas the
radiodensity of air is 1000 HU. The corresponding
value of any material can be calculated by the fol-
lowing equation:
ðmm  mw Þ
CTm ¼ 1000 
mw  ma
where mw, ma, and mm are the attenuation values for
water, air, and the material being measured, respec-
tively. Since ma is nearly zero, the above equation
can be transformed as follows:
 
CTm
mm ¼ 1 þ  mw
1000
Therefore, for a given CT number, for example, a
material in a voxel (the CT unit of volume) is
500 HU, it indicates that mm is 0.5 times of mw.
Assuming that this material only consists of water
and air, we can then conclude that half of the
material in this volume is composed of water and
half is air. Similarly, we can obtain corresponding
gas/water ratio from different CT numbers. Because
the CT number of lung tissue and blood is 20–40
HU, which is close to water, the gas/tissue ratio for a
given voxel from the CT number can be measured.
The different assumptions include that the lungs
only consist of air and tissue (including fluid), and
that the lung structure can be precisely delineated.
Also, the interpretation at the alveolar level will
depend on the size of the voxels. Subsequently, it
is possible to calculate the volume of gas and tissue
for any lung region of interest since the total volume
of this region can be obtained from the numbers of
voxels. Limitations of CT scan for ARDS patients
include the risk of transport, the radiation exposure,
and the time required for quantitative analysis.
Thresholds for recruitment and
hyperinflation
Recent studies have used a whole lung CT scan
instead of a single juxta-diaphragmatic CT section
for quantitative analysis. Lung parenchyma is usually
classified into four compartments, according to the
CT numbers, that is, gas/tissue ratio (Table 1).
Table 1. Classification of lung parenchyma based on different levels of aeration
Type CT numbers
Nonaerated þ100/100 HU
Poorly aerated 101/500 HU
Normally aerated 501/900 HU
Hyperinflated 901/1000 HU
CT, computed tomography; HU, Hounsfield unit.
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Lung volume in ARDS Chen and Brochard
Investigators used thresholds to define non-
aerated and poorly aerated tissue. Gattinoni
et al. [9] first proposed a method to measure
PEEP-induced alveolar recruitment using CT scan
by quantifying the decrease in the weight of non-
aerated lung tissue between two PEEP levels.
Malbouisson et al. [10] proposed to use the increase
in the volume of gas penetrating both nonaerated
and poorly aerated lung regions following PEEP
application. Although debates still exist regarding
these two methods, the quantitative CT-scan
analysis has been considered as a ‘gold standard’
to assess PEEP-induced recruitment.
The CT scan offers a unique opportunity to
quantitate hyperinflation, but it is difficult to define
its threshold. Dambrosio et al. first defined hyper-
inflation in ARDS patients as the lung regions rang-
ing from 800 to 1000 HU, since they found that
the number of voxels between this range increased
by around 10% when PEEP was greater than the
upper inflection point of the volume–pressure
curve. Vieira et al. [11] investigated CT scan in six
healthy volunteers, and found that more than 99%
of lung parenchyma was characterized by CT num-
bers greater than 900 HU at FRC, whereas 30% of
the same lung parenchyma was characterized by CT
numbers ranging between 900 and 1000 HU at a
total lung capacity (TLC). The authors concluded
that 900 HU is a reasonable threshold for hyper-
inflation (i.e. excessive gas/tissue ratio) and ‘over-
distension’. However, whether they really measured
overdistension and whether this can be applied to
patients with edematous lung can be debated. The
cut-off of less than 900 HU has been used for
hyperinflation in most of the following studies.
Using the thresholds in Table 1, Cressoni et al.
&
[12 ] retrospectively analyzed 100 helical CT scans
referred as nonpathological. Patients without lung
disease presented significant percentages of poorly
inflated (18%) and hyperinflated tissue (11%)
during a breath hold at full inspiration (close to
TLC). These findings were quite different from that
of previous studies, and the authors proposed that
age of patients (64  13 years) could be a possible
explanation for the poorly aerated tissue at TLC. The
Gas component Tissue component Gas/tissue ratio
10% 90% 1/9
10.1–50% 50–89.9% 1/9–1
50.1–90% 10–49.9% 1–9
90.1% 9.9% >9
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Cardiopulmonary monitoring
high percentage of hyperinflated tissue may be
explained because CT scans were performed at
TLC. It still, however, raises a doubt about the
threshold 900 HU. The authors used a threshold
950 HU, already used to define pulmonary emphy-
sema, and the hyperinflated tissue was reduced to
around 6%. Nevertheless, the current cut-off com-
monly used (900 HU) or an even lower cut-off
(800 HU) may be more reasonable and safer in
ARDS patients, since for the same CT number (gas/
tissue ratio), it may result in greater alveolar tension
pressure than normal individuals or emphysema-
tous patients. Both the thresholds of hyperinflation
and the relationship between hyperinflation and
regional overdistension (and/or inflammation) still
require further investigations.
Wash-in/washout technique
Instead of measuring gas-diluted concentration
during equilibration, washout technique analyzes
the concentration changes of an inert gas, such
as nitrogen, during washout/wash-in maneuvers.
Olegard et al. [13] proposed a modified nitrogen
washout/wash-in technique, which allowed measur-
ing EELV or FRC (at zero end-expiratory pressure) in
ventilated patients without interruption of mechan-
ical ventilation. This methodology was then inte-
grated in one ventilator and used in experimental
and clinical studies (General Electrics, Wisconsin,
USA). Instead of measuring nitrogen concentration
directly, which requires a mass spectrometer, this
method uses continuous measurement of end-tidal
carbon dioxide (CO2) and oxygen (O2) concen-
trations to calculate the nitrogen concentration.
With a relatively small change in fraction of inspired
oxygen (10–20%), it allows the calculation of the
aerated lung volume during nitrogen washout/wash-
in maneuvers. It has shown good correlations with
helium dilution or CT scan for EELV measurement in
ICU patients [7]. Interestingly, Richard et al. [14]
recently assessed the reliability of this technique at
different levels of PEEP and Vts. The reliability of the
technique was dependent on ventilatory settings, but
was sufficient to accurately detect EELV change
greater than 200 ml. For instance, FRC was very
similar to CT-scan assessment, whereas EELV
measurements significantly differed between the
two techniques at high PEEP levels or Vts above
10 ml/kg. Tang et al. [15] investigated the effect of
alveolar dead space on the accuracy of this technique
for EELV measurement (EELV-N2) during a decre-
mental PEEP trial, in six piglets with lavage-induced
lung injury. They found that in the lower PEEP group
(4–12 cmH2O), EELV-N2 present a high correlation
(r2 ¼ 0.86) with EELV measured by quantitative CT
scan, with a bias of 11 ml; in the higher PEEP group
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(16–20 cmH2O), EELV-N2 was not correlated with
CT, and the bias was negatively correlated with the
alveolar dead space. Another washout technique
using helium with ultrasonic flow meter has shown
an excellent correlation and close agreement with the
CT-scan technique for EELV in rabbits [16]. Inde-
pendent from the tracing gases, the accuracy of the
washout technique for measurement of EELV may be
reduced during high PEEP (>13–14 cmH2O), rapid
breathing, and/or large Vt. It, however, provides a
noninvasive, well tolerated, repeatable method to
measure FRC and EELV at the bedside.
DYNAMIC CHANGES IN LUNG VOLUME
The noninvasive, radiation-free imaging technique
of electrical impedance tomography (EIT) has
been increasingly investigated as a new tool to
monitor global and regional changes in lung
volumes at the bedside. The technique measures
regional changes in tissue impedance at a cross-
sectional slice of the thorax, with probes placed
on the body surface. An experimental study
performed by Frerichs et al. [17] demonstrated a
good correlation between the regional changes in
lung gas volume determined by EIT and CT scan. EIT
has been found as a useful tool for monitoring the
regional distribution of Vt in the clinical settings
[18], but results are conflicting. A recent clinical
study supported that the cross-sectional lung
volume changes measured by EIT were representa-
tive for the whole lung [19]. The technique seems to
have the ability to semiquantitatively assess the
changes in EELV (DEELV) and recruitment/dere-
cruitment during the PEEP trial [20,21]. During a
PEEP trial, however, one study found that the esti-
mation of DEELV was found unreliable because
impedance is measured only at one level above
the diaphragm [22]. Further studies need to be
carried out before applying this promising techno-
logy into routine practice. Also, Karsten et al. [23]
showed that during different respiratory maneuvers
like endotracheal suctioning or recruitment
maneuvers, EELV could not be estimated by EIT
with reasonable accuracy.
SPECIFIC CLINICAL INDICATIONS
Two major clinical applications of lung volume
measurement include the use of EELV to evaluate
the effects of interventions and the use of strain as a
clinical monitoring index.
Positioning
Using the quantification of recruitment and hyper-
inflation using CT scan in 24 patients with ARDS,
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&&
Cornejo et al. [24 ] clearly observed that high PEEP
not only led to lung recruitment but also increased
hyperinflation. They found that prone positioning
enhanced the benefit of high PEEP in terms of
recruitment and prevented the negative impact of
PEEP on hyperinflation. Moreover, a combined use
of high PEEP and prone positioning decreased
cyclic recruitment/derecruitment, especially in
highly recruitable patients. This is important since
this cyclic opening and closure is one of the main
mechanisms for inducing ventilator-induced lung
injury (VILI).
&
Dellamonica et al. [25 ] evaluated whether ver-
ticalization had parallel effects on oxygenation and
EELV using nitrogen washout/wash-in technique
in 40 patients with ARDS. They found that both
PaO2/FiO2 ratio and EELV/PBW were significantly
higher in seated than in supine position. Strain also
decreased with verticalization in responders defined
as 20% or more increase in PaO2/FiO2 between the
supine and the seated positions. EELV/PBW increase
and PaO2/FiO2 increase were not correlated. An
increase in EELV during verticalization does not
necessarily mean that there is an increase in recruit-
ment, since EELV is composed of both FRC and
PEEP-induced DEELV. FRC may significantly change
during verticalization, and the PEEP-induced DEELV
also depends on the respiratory system compliance
at different positions.
Pleural effusion
Two independent groups [26,27] investigated the
physiological effects of pleural effusion and the
effects of drainage on EELV, using CT-scan tech-
nique and nitrogen washout/wash-in technique,
respectively. Chiumello et al. [27] demonstrated that
pleural effusion in ARDS patients leads to a greater
chest wall expansion than lung reduction in terms
of EELV. Razazi et al. [26] found in ventilated
patients with large (500 ml) pleural effusion that
an improvement in PaO2/FiO2 ratio from baseline to
24 h was positively correlated with the increase in
EELV and the change in transpulmonary pressure
after drainage, but not with drained fluid volume.
The benefits of drainage on these parameters was
less pronounced in patients with ARDS, suggesting
that taking the risk of pleural drainage may not be
warranted in ARDS, whereas it may be more inter-
esting regarding weaning from mechanical venti-
lation.
Intra-abdominal hypertension
The influence of intra-abdominal hypertension on
transpulmonary pressure, lung volume, and lung
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Lung volume in ARDS Chen and Brochard
injury has been the subject of many investigations.
One important clinical question is how this should
affect ventilatory settings. It has been suggested that
clinicians could target higher threshold for plateau
pressure in case of intra-abdominal hypertension
[28]. Regli et al. [29] found that in a pig model of
intra-abdominal hypertension, PEEP matched to
intra-abdominal pressure led to a preservation of
EELV, but did not improve oxygenation and caused
a reduction in cardiac output.
Atelectasis
Whether changes in oxygenation reflect improve-
ment in atelectasis was evaluated in 21 patients
with atelectasis under mechanical ventilation and
submitted to different recruitment maneuvers by
Nakahashi et al. [30]. They demonstrated that the
DEELV was correlated with the DPaO2/FiO2 ratio and
was identified as an accurate predictor of the
improvement of oxygenation during recruitment
maneuver for patients with atelectasis.
Strain
The concept of strain is attractive because it could
potentially be used to dictate our ventilatory
settings in limiting the end-inspiratory lung
volume in relation to the initial FRC. Liu et al.
[31] established animal models of ARDS to investi-
gate whether lung stress and strain can be surro-
gated by airway plateau pressure (Pplat) and Vt,
respectively. The results showed a good linear
relationship between lung stress and Pplat in healthy
and ARDS lungs, whereas for a given Vt (10 ml/kg),
the strain varied remarkably in healthy and ARDS
lungs. Gonzalez-Lopez et al. [32] compared 16 ARDS
patients with six non-ARDS ventilated patients
(control). Strain was computed as tidal volume/
EELV. Patients in the ARDS group exhibited higher
airway pressure, lower EELV, and higher strain than
those in the control group, whereas Vt and gas
exchange were similar. The subgroup of patients
with high strain demonstrated a four-fold increase
of IL-6 and IL-8 concentrations in bronchoalveolar
lavage fluid, compared to patients with ‘normal’
strain, that is, lower than the median, whether or
not they had ARDS. This suggests that increased
strain is associated with a pro-inflammatory lung
response.
CONCLUSION
Lung volume measurements constitute an import-
ant advance for monitoring and potentially for the
management of patients with ARDS. Recent progress
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Cardiopulmonary monitoring
in technology allows clinicians to evaluate static/
dynamic lung volumes noninvasively at the bed-
side, whereas quantitative CT-scan analysis remains
the ‘most powerful’ and also the ‘most complex’
reference technique.
Acknowledgements
None.
Financial support and sponsorship
None.
Conflicts of interest
Dr Laurent Brochard has received research grants from
Draeger, General Electric, Covidien, Vygon, Fisher Pay-
kel and personal fees from Covidien, outside the sub-
mitted work. He has also developed an educational tool
on lung volume with General Electric. Dr Lu Chen has no
conflict of interest.
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Volume 21
Number 3
June 2015