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

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Cardiopulmonary monitoring

Limited use in clinical practice


KEY POINTS Despite its strong potential clinical interest, assess-
 Lung volume measurements represent a strong potential ment of lung volume at the bedside is limited due to
clinical interest for individualization of ventilator settings the complexities of the techniques used in the past.
to reduce the risks of ventilator-induced lung injury in Recent progress in technology may facilitate the
patients with ARDS. application of either absolute lung volume measure-
ments or changes in lung volume. We will summar-
 Quantitative measurements of static lung volumes can
provide valuable information and have become easier ize the current techniques available for lung volume
to use in clinical practice. assessment in the ICU and the recent findings
obtained with implementation of these techniques
 Data indicate that the reliability of lung volume in patients with ARDS.
measurements may depend on ventilatory settings.
 Electrical impedance tomography has been
increasingly investigated as a new tool to ABSOLUTE LUNG VOLUMES
semiquantitatively assess dynamic changes in lung Three types of techniques are available for measur-
volumes at the bedside. ing the absolute or static lung volumes in patients
with ARDS.

for all patients with ARDS. Recent studies indicated Gas dilution technique
that the risk of Vt-induced overdistension or volu- Gas dilution technique has been applied to measure
trauma depends on the amount of aerated tissue static lung volumes for more than two centuries. It is
receiving the gas. A term from the field of contin- based on equilibration of gas in the lung with a
uum mechanics – strain – has been used to describe known volume of gas containing a known fraction
the lung deformation related to its original status: of an inert gas. The multibreath helium equili-
Vt-induced strain is the ratio of Vt to functional bration technique has been used as a common
residual capacity (FRC). Consequently, the same method for measuring FRC in pulmonary function
Vt/PBW may generate much greater strain in case test laboratory, but was essentially used for clinical
of low FRC than with high FRC; 6 ml/kg still may be research in mechanically ventilated patients due to
excessive in a patient with extremely reduced FRC technical complexity. Pesenti’s group proposed a
and may be unnecessarily low in a patient with a simplified helium dilution method in terms of
well preserved FRC, at the price of deep sedation or instrumentation. They concluded that this simpli-
paralysis. Therefore, individualized setting of Vt fied helium dilution method is clinically acceptable
based on strain seems physiologically sound and when applied in ventilated patients with a short
of potential benefit. This approach requires a valid time constant of the respiratory system, such as
measurement of FRC. ARDS patients [6,7]. A dilution technique using
methane is also possible [8], but neither these sim-
plified techniques nor the classical helium dilution
Positive end-expiratory pressure and technique can be performed without disconnection
recruitment from the ventilator or without the use of relatively
Positive end-expiratory pressure (PEEP) has been cumbersome equipment. Because of its complexity,
applied in patients with ARDS for the purpose of gas dilution technique is still limited to research
recruiting collapsed lung tissue, or more exactly for purpose in ARDS.
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: Computed tomography scan technique
recruitment of previously non/poorly aerated Quantitative analysis of computed tomography
tissue, and inflation or hyperinflation of previously (CT) scans enables an accurate evaluation of the
normally aerated tissue. For example, in a highly volume of gas and tissue in the lungs of ARDS
recruitable patient, a large amount of the increase patients. It is based on the linear correlation
in EELV is caused by reopening of previously between the X-ray attenuation in a given volume
collapsed lung tissue, whereas in a poorly recruitable and the physical density of that volume, namely,
patient, the increase in EELV is generated by the radiodensity. The Hounsfield unit scale (HU) or
inflation of previously open lung tissue which CT numbers is a quantitative scale for describing
may lead to hyperinflation. Therefore, the effec- radiodensity. It refers to a dimensionless index of
tiveness of PEEP depends on assessment of recruit- X-ray attenuation that is related to the attenuation
ability. of air and water, with an arbitrary allocation of the

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Lung volume in ARDS Chen and Brochard

radiodensity of distilled water to 0 HU, whereas the Investigators used thresholds to define non-
radiodensity of air is 1000 HU. The corresponding aerated and poorly aerated tissue. Gattinoni
value of any material can be calculated by the fol- et al. [9] first proposed a method to measure
lowing equation: PEEP-induced alveolar recruitment using CT scan
ðmm  mw Þ by quantifying the decrease in the weight of non-
CTm ¼ 1000  aerated lung tissue between two PEEP levels.
mw  ma
Malbouisson et al. [10] proposed to use the increase
in the volume of gas penetrating both nonaerated
where mw, ma, and mm are the attenuation values for
and poorly aerated lung regions following PEEP
water, air, and the material being measured, respec-
application. Although debates still exist regarding
tively. Since ma is nearly zero, the above equation
these two methods, the quantitative CT-scan
can be transformed as follows:
  analysis has been considered as a ‘gold standard’
CTm to assess PEEP-induced recruitment.
mm ¼ 1 þ  mw
1000 The CT scan offers a unique opportunity to
quantitate hyperinflation, but it is difficult to define
Therefore, for a given CT number, for example, a its threshold. Dambrosio et al. first defined hyper-
material in a voxel (the CT unit of volume) is inflation in ARDS patients as the lung regions rang-
500 HU, it indicates that mm is 0.5 times of mw. ing from 800 to 1000 HU, since they found that
Assuming that this material only consists of water the number of voxels between this range increased
and air, we can then conclude that half of the by around 10% when PEEP was greater than the
material in this volume is composed of water and upper inflection point of the volume–pressure
half is air. Similarly, we can obtain corresponding curve. Vieira et al. [11] investigated CT scan in six
gas/water ratio from different CT numbers. Because healthy volunteers, and found that more than 99%
the CT number of lung tissue and blood is 20–40 of lung parenchyma was characterized by CT num-
HU, which is close to water, the gas/tissue ratio for a bers greater than 900 HU at FRC, whereas 30% of
given voxel from the CT number can be measured. the same lung parenchyma was characterized by CT
The different assumptions include that the lungs numbers ranging between 900 and 1000 HU at a
only consist of air and tissue (including fluid), and total lung capacity (TLC). The authors concluded
that the lung structure can be precisely delineated. that 900 HU is a reasonable threshold for hyper-
Also, the interpretation at the alveolar level will inflation (i.e. excessive gas/tissue ratio) and ‘over-
depend on the size of the voxels. Subsequently, it distension’. However, whether they really measured
is possible to calculate the volume of gas and tissue overdistension and whether this can be applied to
for any lung region of interest since the total volume patients with edematous lung can be debated. The
of this region can be obtained from the numbers of cut-off of less than 900 HU has been used for
voxels. Limitations of CT scan for ARDS patients hyperinflation in most of the following studies.
include the risk of transport, the radiation exposure, Using the thresholds in Table 1, Cressoni et al.
and the time required for quantitative analysis. &
[12 ] retrospectively analyzed 100 helical CT scans
referred as nonpathological. Patients without lung
Thresholds for recruitment and disease presented significant percentages of poorly
hyperinflation inflated (18%) and hyperinflated tissue (11%)
Recent studies have used a whole lung CT scan during a breath hold at full inspiration (close to
instead of a single juxta-diaphragmatic CT section TLC). These findings were quite different from that
for quantitative analysis. Lung parenchyma is usually of previous studies, and the authors proposed that
classified into four compartments, according to the age of patients (64  13 years) could be a possible
CT numbers, that is, gas/tissue ratio (Table 1). explanation for the poorly aerated tissue at TLC. The

Table 1. Classification of lung parenchyma based on different levels of aeration

Type CT numbers Gas component Tissue component Gas/tissue ratio

Nonaerated þ100/100 HU 10% 90% 1/9


Poorly aerated 101/500 HU 10.1–50% 50–89.9% 1/9–1
Normally aerated 501/900 HU 50.1–90% 10–49.9% 1–9
Hyperinflated 901/1000 HU 90.1% 9.9% >9

CT, computed tomography; HU, Hounsfield unit.

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high percentage of hyperinflated tissue may be (16–20 cmH2O), EELV-N2 was not correlated with
explained because CT scans were performed at CT, and the bias was negatively correlated with the
TLC. It still, however, raises a doubt about the alveolar dead space. Another washout technique
threshold 900 HU. The authors used a threshold using helium with ultrasonic flow meter has shown
950 HU, already used to define pulmonary emphy- an excellent correlation and close agreement with the
sema, and the hyperinflated tissue was reduced to CT-scan technique for EELV in rabbits [16]. Inde-
around 6%. Nevertheless, the current cut-off com- pendent from the tracing gases, the accuracy of the
monly used (900 HU) or an even lower cut-off washout technique for measurement of EELV may be
(800 HU) may be more reasonable and safer in reduced during high PEEP (>13–14 cmH2O), rapid
ARDS patients, since for the same CT number (gas/ breathing, and/or large Vt. It, however, provides a
tissue ratio), it may result in greater alveolar tension noninvasive, well tolerated, repeatable method to
pressure than normal individuals or emphysema- measure FRC and EELV at the bedside.
tous patients. Both the thresholds of hyperinflation
and the relationship between hyperinflation and
regional overdistension (and/or inflammation) still DYNAMIC CHANGES IN LUNG VOLUME
require further investigations. The noninvasive, radiation-free imaging technique
of electrical impedance tomography (EIT) has
Wash-in/washout technique been increasingly investigated as a new tool to
Instead of measuring gas-diluted concentration monitor global and regional changes in lung
during equilibration, washout technique analyzes volumes at the bedside. The technique measures
the concentration changes of an inert gas, such regional changes in tissue impedance at a cross-
as nitrogen, during washout/wash-in maneuvers. sectional slice of the thorax, with probes placed
Olegard et al. [13] proposed a modified nitrogen on the body surface. An experimental study
washout/wash-in technique, which allowed measur- performed by Frerichs et al. [17] demonstrated a
ing EELV or FRC (at zero end-expiratory pressure) in good correlation between the regional changes in
ventilated patients without interruption of mechan- lung gas volume determined by EIT and CT scan. EIT
ical ventilation. This methodology was then inte- has been found as a useful tool for monitoring the
grated in one ventilator and used in experimental regional distribution of Vt in the clinical settings
and clinical studies (General Electrics, Wisconsin, [18], but results are conflicting. A recent clinical
USA). Instead of measuring nitrogen concentration study supported that the cross-sectional lung
directly, which requires a mass spectrometer, this volume changes measured by EIT were representa-
method uses continuous measurement of end-tidal tive for the whole lung [19]. The technique seems to
carbon dioxide (CO2) and oxygen (O2) concen- have the ability to semiquantitatively assess the
trations to calculate the nitrogen concentration. changes in EELV (DEELV) and recruitment/dere-
With a relatively small change in fraction of inspired cruitment during the PEEP trial [20,21]. During a
oxygen (10–20%), it allows the calculation of the PEEP trial, however, one study found that the esti-
aerated lung volume during nitrogen washout/wash- mation of DEELV was found unreliable because
in maneuvers. It has shown good correlations with impedance is measured only at one level above
helium dilution or CT scan for EELV measurement in the diaphragm [22]. Further studies need to be
ICU patients [7]. Interestingly, Richard et al. [14] carried out before applying this promising techno-
recently assessed the reliability of this technique at logy into routine practice. Also, Karsten et al. [23]
different levels of PEEP and Vts. The reliability of the showed that during different respiratory maneuvers
technique was dependent on ventilatory settings, but like endotracheal suctioning or recruitment
was sufficient to accurately detect EELV change maneuvers, EELV could not be estimated by EIT
greater than 200 ml. For instance, FRC was very with reasonable accuracy.
similar to CT-scan assessment, whereas EELV
measurements significantly differed between the
two techniques at high PEEP levels or Vts above SPECIFIC CLINICAL INDICATIONS
10 ml/kg. Tang et al. [15] investigated the effect of Two major clinical applications of lung volume
alveolar dead space on the accuracy of this technique measurement include the use of EELV to evaluate
for EELV measurement (EELV-N2) during a decre- the effects of interventions and the use of strain as a
mental PEEP trial, in six piglets with lavage-induced clinical monitoring index.
lung injury. They found that in the lower PEEP group
(4–12 cmH2O), EELV-N2 present a high correlation Positioning
(r2 ¼ 0.86) with EELV measured by quantitative CT Using the quantification of recruitment and hyper-
scan, with a bias of 11 ml; in the higher PEEP group inflation using CT scan in 24 patients with ARDS,

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Lung volume in ARDS Chen and Brochard

&&
Cornejo et al. [24 ] clearly observed that high PEEP injury has been the subject of many investigations.
not only led to lung recruitment but also increased One important clinical question is how this should
hyperinflation. They found that prone positioning affect ventilatory settings. It has been suggested that
enhanced the benefit of high PEEP in terms of clinicians could target higher threshold for plateau
recruitment and prevented the negative impact of pressure in case of intra-abdominal hypertension
PEEP on hyperinflation. Moreover, a combined use [28]. Regli et al. [29] found that in a pig model of
of high PEEP and prone positioning decreased intra-abdominal hypertension, PEEP matched to
cyclic recruitment/derecruitment, especially in intra-abdominal pressure led to a preservation of
highly recruitable patients. This is important since EELV, but did not improve oxygenation and caused
this cyclic opening and closure is one of the main a reduction in cardiac output.
mechanisms for inducing ventilator-induced lung
injury (VILI).
&
Dellamonica et al. [25 ] evaluated whether ver- Atelectasis
ticalization had parallel effects on oxygenation and Whether changes in oxygenation reflect improve-
EELV using nitrogen washout/wash-in technique ment in atelectasis was evaluated in 21 patients
in 40 patients with ARDS. They found that both with atelectasis under mechanical ventilation and
PaO2/FiO2 ratio and EELV/PBW were significantly submitted to different recruitment maneuvers by
higher in seated than in supine position. Strain also Nakahashi et al. [30]. They demonstrated that the
decreased with verticalization in responders defined DEELV was correlated with the DPaO2/FiO2 ratio and
as 20% or more increase in PaO2/FiO2 between the was identified as an accurate predictor of the
supine and the seated positions. EELV/PBW increase improvement of oxygenation during recruitment
and PaO2/FiO2 increase were not correlated. An maneuver for patients with atelectasis.
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 Strain
PEEP-induced DEELV. FRC may significantly change The concept of strain is attractive because it could
during verticalization, and the PEEP-induced DEELV potentially be used to dictate our ventilatory
also depends on the respiratory system compliance settings in limiting the end-inspiratory lung
at different positions. 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-
Pleural effusion gated by airway plateau pressure (Pplat) and Vt,
Two independent groups [26,27] investigated the respectively. The results showed a good linear
physiological effects of pleural effusion and the relationship between lung stress and Pplat in healthy
effects of drainage on EELV, using CT-scan tech- and ARDS lungs, whereas for a given Vt (10 ml/kg),
nique and nitrogen washout/wash-in technique, the strain varied remarkably in healthy and ARDS
respectively. Chiumello et al. [27] demonstrated that lungs. Gonzalez-Lopez et al. [32] compared 16 ARDS
pleural effusion in ARDS patients leads to a greater patients with six non-ARDS ventilated patients
chest wall expansion than lung reduction in terms (control). Strain was computed as tidal volume/
of EELV. Razazi et al. [26] found in ventilated EELV. Patients in the ARDS group exhibited higher
patients with large (500 ml) pleural effusion that airway pressure, lower EELV, and higher strain than
an improvement in PaO2/FiO2 ratio from baseline to those in the control group, whereas Vt and gas
24 h was positively correlated with the increase in exchange were similar. The subgroup of patients
EELV and the change in transpulmonary pressure with high strain demonstrated a four-fold increase
after drainage, but not with drained fluid volume. of IL-6 and IL-8 concentrations in bronchoalveolar
The benefits of drainage on these parameters was lavage fluid, compared to patients with ‘normal’
less pronounced in patients with ARDS, suggesting strain, that is, lower than the median, whether or
that taking the risk of pleural drainage may not be not they had ARDS. This suggests that increased
warranted in ARDS, whereas it may be more inter- strain is associated with a pro-inflammatory lung
esting regarding weaning from mechanical venti- response.
lation.

CONCLUSION
Intra-abdominal hypertension Lung volume measurements constitute an import-
The influence of intra-abdominal hypertension on ant advance for monitoring and potentially for the
transpulmonary pressure, lung volume, and lung management of patients with ARDS. Recent progress

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Cardiopulmonary monitoring

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in technology allows clinicians to evaluate static/ & thoracic CT analysis. Crit Care 2013; 17:R93.
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