REVIEW URRENT C 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 proinflammatory 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 Acute respiratory distress syndrome (ARDS) is characterized by various degrees of reduction in aerated lung volume due to alveolar flooding, consolidation, 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
‘volutrauma’ [4]. Because of the reduction of aerated lung volume in ARDS, the need to ventilate the lungs with lower tidal volume (Vt) than conventional setting (10–15 ml/kg) or even than normal individuals (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. However, 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: [email protected] Curr Opin Crit Care 2015, 21:259–264 DOI:10.1097/MCC.0000000000000193
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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 volutrauma depends on the amount of aerated tissue receiving the gas. A term from the field of continuum 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 consequence 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 effectiveness of PEEP depends on assessment of recruitability. 260
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Limited use in clinical practice Despite its strong potential clinical interest, assessment 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 measurements or changes in lung volume. We will summarize 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 measuring 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 equilibration 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 simplified 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 simplified 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 Volume 21 Number 3 June 2015
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Lung volume in ARDS Chen and Brochard
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 following equation: CTm ¼ 1000
ðmm mw Þ mw ma
where mw, ma, and mm are the attenuation values for water, air, and the material being measured, respectively. 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).
Investigators used thresholds to define nonaerated 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 nonaerated 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 hyperinflation in ARDS patients as the lung regions ranging 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 numbers 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 hyperinflation (i.e. excessive gas/tissue ratio) and ‘overdistension’. 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 &
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
901/1000 HU
90.1%
9.9%
>9
Hyperinflated
CT, computed tomography; HU, Hounsfield unit.
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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 emphysema, and the hyperinflated tissue was reduced to around 6%. Nevertheless, the current cut-off commonly 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 emphysematous 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 measuring EELV or FRC (at zero end-expiratory pressure) in ventilated patients without interruption of mechanical ventilation. This methodology was then integrated 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) concentrations 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/washin 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 decremental 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 262
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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]. Independent 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 crosssectional 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 representative for the whole lung [19]. The technique seems to have the ability to semiquantitatively assess the changes in EELV (DEELV) and recruitment/derecruitment during the PEEP trial [20,21]. During a PEEP trial, however, one study found that the estimation 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 technology 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 hyperinflation using CT scan in 24 patients with ARDS, Volume 21 Number 3 June 2015
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Lung volume in ARDS Chen and Brochard &&
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 verticalization 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 recruitment, 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 technique 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 interesting regarding weaning from mechanical ventilation.
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 improvement 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 investigate whether lung stress and strain can be surrogated 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 Intra-abdominal hypertension The influence of intra-abdominal hypertension on transpulmonary pressure, lung volume, and lung
Lung volume measurements constitute an important advance for monitoring and potentially for the management of patients with ARDS. Recent progress
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in technology allows clinicians to evaluate static/ dynamic lung volumes noninvasively at the bedside, 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 Paykel and personal fees from Covidien, outside the submitted work. He has also developed an educational tool on lung volume with General Electric. Dr Lu Chen has no conflict of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Falke KJ, Pontoppidan H, Kumar A, et al. Ventilation with end-expiratory pressure in acute lung disease. J Clin Invest 1972; 51:2315–2323. 2. Suter PM, Fairley B, Isenberg MD. Optimum end-expiratory airway pressure in patients with acute pulmonary failure. N Engl J Med 1975; 292:284–289. 3. Dreyfuss D, Soler P, Basset G, Saumon G. High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Resp Dis 1988; 137:1159–1164. 4. Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 1998; 157:294–323. 5. ARDSnet. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. New Engl J Med 2000; 342:1301–1308. 6. Patroniti N, Bellani G, Manfio A, et al. Lung volume in mechanically ventilated patients: measurement by simplified helium dilution compared to quantitative CT scan. Intensive Care Med 2004; 30:282–289. 7. Chiumello D, Cressoni M, Chierichetti M, et al. Nitrogen washout/washin, helium dilution and computed tomography in the assessment of end expiratory lung volume. Crit Care (London, England) 2008; 12:R150. 8. Pinto Da Costa N, Di Marco F, Lyazidi A, et al. Effect of pressure support on end-expiratory lung volume and lung diffusion for carbon monoxide. Crit Care Med 2011; 39:2283–2289. 9. Gattinoni L, Pelosi P, Crotti S, Valenza F. Effects of positive end-expiratory pressure on regional distribution of tidal volume and recruitment in adultrespiratory-distress-syndrome. Am J Respir Crit Care Med 1995; 151:1807– 1814. 10. Malbouisson LM, Muller JC, Constantin JM, et al. Computed tomography assessment of positive end-expiratory pressure-induced alveolar recruitment in patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2001; 163:1444–1450. 11. Vieira SR, Puybasset L, Richecoeur J, et al. A lung computed tomographic assessment of positive end-expiratory pressure-induced lung overdistension. Am J Respir Crit Care Med 1998; 158:1571–1577.
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12. Cressoni M, Gallazzi E, Chiurazzi C, et al. Limits of normality of quantitative thoracic CT analysis. Crit Care 2013; 17:R93. This retrospective analysis using CT-scan technique demonstrated surprising results in distribution of aeration in nonpathological lungs, which need further discussions and investigations. 13. Olegard C, Sondergaard S, Houltz E, et al. Estimation of functional residual capacity at the bedside using standard monitoring equipment: a modified nitrogen washout/washin technique requiring a small change of the inspired oxygen fraction. Anesth Analg 2005; 101:206–212. 14. Richard JC, Pouzot C, Pinzon AM. Reliability of the nitrogen washin-washout technique to assess end-expiratory lung volume at variable peep and tidal volumes. Intensive Care Med Exp 2014; 2:10. 15. Tang R, Huang YZ, Chen QH, et al. The effect of alveolar dead space on the measurement of end-expiratory lung volume by modified nitrogen wash-out/ wash-in in lavage-induced lung injury. Respir Care 2012; 57:2074–2081. 16. Albu G, Petak F, Zand T, et al. Lung volume assessments in normal and surfactant depleted lungs: Agreement between bedside techniques and CT imaging. BMC Anesthesiol 2014; 14:64. 17. Frerichs I, Hinz J, Herrmann P, et al. Detection of local lung air content by electrical impedance tomography compared with electron beam CT. J Appl Physiol 2002; 93:660–666. 18. Yoshida T, Torsani V, Gomes S, et al. Spontaneous effort causes occult pendelluft during mechanical ventilation. Am J Respir Crit Care Med 2013; 188:1420–1427. 19. van der Burg PS, Miedema M, de Jongh FH, et al. Cross-sectional changes in lung volume measured by electrical impedance tomography are representative for the whole lung in ventilated preterm infants. Crit Care Med 2014; 42:1524–1530. 20. Hinz J, Hahn G, Neumann P, et al. End-expiratory lung impedance change enables bedside monitoring of end-expiratory lung volume change. Intensive Care Med 2003; 29:37–43. 21. Meier T, Luepschen H, Karsten J, et al. Assessment of regional lung recruitment and derecruitment during a PEEP trial based on electrical impedance tomography. Intensive Care Med 2008; 34:543–550. 22. Bikker IG, Leonhardt S, Bakker J, Gommers D. Lung volume calculated from electrical impedance tomography in icu patients at different peep levels. Intensive Care Med 2009; 35:1362–1367. 23. Karsten J, Meier T, Iblher P, et al. The suitability of EIT to estimate EELV in a clinical trial compared to oxygen wash-in/wash-out technique. Biomedizinische Technik Biomedical Engin 2014; 59:59–64. 24. Cornejo RA, Diaz JC, Tobar EA, et al. Effects of prone positioning on lung && protection in patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2013; 188:440–448. This study investigated the effect of prone position on the different volumes (hyperinflated, normally aerated and poorly or non aerated) as estimated by CT scan in ARDS patients, as well as the protective effect on tidal recruitment. 25. Dellamonica J, Lerolle N, Sargentini C, et al. Effect of different seated & positions on lung volume and oxygenation in acute respiratory distress syndrome. Intensive Care Med 2013; 39:1121–1127. This physiological study indicated significant increase in EELV and decrease in strain during verticalization. 26. Razazi K, Thille AW, Carteaux G, et al. Effects of pleural effusion drainage on oxygenation, respiratory mechanics, and hemodynamics in mechanically ventilated patients. Annals Am Thor Soc 2014; 11:1018–1024. 27. Chiumello D, Marino A, Cressoni M, et al. Pleural effusion in patients with acute lung injury: a CT scan study. Crit Care Med 2013; 41:935–944. 28. Cortes-Puentes GA, Cortes-Puentes LA, Adams AB, et al. Experimental intra-abdominal hypertension influences airway pressure limits for lung protective mechanical ventilation. J Trauma Acute Care Surg 2013; 74:1468– 1473. 29. Regli A, Chakera J, De Keulenaer BL, et al. Matching positive end-expiratory pressure to intra-abdominal pressure prevents end-expiratory lung volume decline in a pig model of intra-abdominal hypertension. Crit Care Med 2012; 40:1879–1886. 30. Nakahashi S, Gando S, Ishikawa T, et al. Effectiveness of end-expiratory lung volume measurements during the lung recruitment maneuver for patients with atelectasis. J Crit Care 2013; 28:534.e1-5. 31. Liu Q, Li W, Zeng QS, et al. Lung stress and strain during mechanical ventilation in animals with and without pulmonary acute respiratory distress syndrome. J Surg Res 2013; 181:300–307. 32. Gonzalez-Lopez A, Garcia-Prieto E, Batalla-Solis E, et al. Lung strain and biological response in mechanically ventilated patients. Intensive Care Med 2012; 38:240–247. &
Volume 21 Number 3 June 2015
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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 proinflammatory 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 Acute respiratory distress syndrome (ARDS) is characterized by various degrees of reduction in aerated lung volume due to alveolar flooding, consolidation, 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
‘volutrauma’ [4]. Because of the reduction of aerated lung volume in ARDS, the need to ventilate the lungs with lower tidal volume (Vt) than conventional setting (10–15 ml/kg) or even than normal individuals (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. However, 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: [email protected] Curr Opin Crit Care 2015, 21:259–264 DOI:10.1097/MCC.0000000000000193
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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 volutrauma depends on the amount of aerated tissue receiving the gas. A term from the field of continuum 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 consequence 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 effectiveness of PEEP depends on assessment of recruitability. 260
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Limited use in clinical practice Despite its strong potential clinical interest, assessment 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 measurements or changes in lung volume. We will summarize 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 measuring 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 equilibration 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 simplified 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 simplified 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 Volume 21 Number 3 June 2015
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Lung volume in ARDS Chen and Brochard
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 following equation: CTm ¼ 1000
ðmm mw Þ mw ma
where mw, ma, and mm are the attenuation values for water, air, and the material being measured, respectively. 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).
Investigators used thresholds to define nonaerated 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 nonaerated 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 hyperinflation in ARDS patients as the lung regions ranging 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 numbers 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 hyperinflation (i.e. excessive gas/tissue ratio) and ‘overdistension’. 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 &
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
901/1000 HU
90.1%
9.9%
>9
Hyperinflated
CT, computed tomography; HU, Hounsfield unit.
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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 emphysema, and the hyperinflated tissue was reduced to around 6%. Nevertheless, the current cut-off commonly 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 emphysematous 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 measuring EELV or FRC (at zero end-expiratory pressure) in ventilated patients without interruption of mechanical ventilation. This methodology was then integrated 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) concentrations 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/washin 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 decremental 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 262
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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]. Independent 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 crosssectional 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 representative for the whole lung [19]. The technique seems to have the ability to semiquantitatively assess the changes in EELV (DEELV) and recruitment/derecruitment during the PEEP trial [20,21]. During a PEEP trial, however, one study found that the estimation 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 technology 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 hyperinflation using CT scan in 24 patients with ARDS, Volume 21 Number 3 June 2015
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Lung volume in ARDS Chen and Brochard &&
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 verticalization 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 recruitment, 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 technique 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 interesting regarding weaning from mechanical ventilation.
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 improvement 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 investigate whether lung stress and strain can be surrogated 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 Intra-abdominal hypertension The influence of intra-abdominal hypertension on transpulmonary pressure, lung volume, and lung
Lung volume measurements constitute an important advance for monitoring and potentially for the management of patients with ARDS. Recent progress
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in technology allows clinicians to evaluate static/ dynamic lung volumes noninvasively at the bedside, 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 Paykel and personal fees from Covidien, outside the submitted work. He has also developed an educational tool on lung volume with General Electric. Dr Lu Chen has no conflict of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Falke KJ, Pontoppidan H, Kumar A, et al. Ventilation with end-expiratory pressure in acute lung disease. J Clin Invest 1972; 51:2315–2323. 2. Suter PM, Fairley B, Isenberg MD. Optimum end-expiratory airway pressure in patients with acute pulmonary failure. N Engl J Med 1975; 292:284–289. 3. Dreyfuss D, Soler P, Basset G, Saumon G. High inflation pressure pulmonary edema. Respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Resp Dis 1988; 137:1159–1164. 4. Dreyfuss D, Saumon G. Ventilator-induced lung injury: lessons from experimental studies. Am J Respir Crit Care Med 1998; 157:294–323. 5. ARDSnet. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. New Engl J Med 2000; 342:1301–1308. 6. Patroniti N, Bellani G, Manfio A, et al. Lung volume in mechanically ventilated patients: measurement by simplified helium dilution compared to quantitative CT scan. Intensive Care Med 2004; 30:282–289. 7. Chiumello D, Cressoni M, Chierichetti M, et al. Nitrogen washout/washin, helium dilution and computed tomography in the assessment of end expiratory lung volume. Crit Care (London, England) 2008; 12:R150. 8. Pinto Da Costa N, Di Marco F, Lyazidi A, et al. Effect of pressure support on end-expiratory lung volume and lung diffusion for carbon monoxide. Crit Care Med 2011; 39:2283–2289. 9. Gattinoni L, Pelosi P, Crotti S, Valenza F. Effects of positive end-expiratory pressure on regional distribution of tidal volume and recruitment in adultrespiratory-distress-syndrome. Am J Respir Crit Care Med 1995; 151:1807– 1814. 10. Malbouisson LM, Muller JC, Constantin JM, et al. Computed tomography assessment of positive end-expiratory pressure-induced alveolar recruitment in patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2001; 163:1444–1450. 11. Vieira SR, Puybasset L, Richecoeur J, et al. A lung computed tomographic assessment of positive end-expiratory pressure-induced lung overdistension. Am J Respir Crit Care Med 1998; 158:1571–1577.
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12. Cressoni M, Gallazzi E, Chiurazzi C, et al. Limits of normality of quantitative thoracic CT analysis. Crit Care 2013; 17:R93. This retrospective analysis using CT-scan technique demonstrated surprising results in distribution of aeration in nonpathological lungs, which need further discussions and investigations. 13. Olegard C, Sondergaard S, Houltz E, et al. Estimation of functional residual capacity at the bedside using standard monitoring equipment: a modified nitrogen washout/washin technique requiring a small change of the inspired oxygen fraction. Anesth Analg 2005; 101:206–212. 14. Richard JC, Pouzot C, Pinzon AM. Reliability of the nitrogen washin-washout technique to assess end-expiratory lung volume at variable peep and tidal volumes. Intensive Care Med Exp 2014; 2:10. 15. Tang R, Huang YZ, Chen QH, et al. The effect of alveolar dead space on the measurement of end-expiratory lung volume by modified nitrogen wash-out/ wash-in in lavage-induced lung injury. Respir Care 2012; 57:2074–2081. 16. Albu G, Petak F, Zand T, et al. Lung volume assessments in normal and surfactant depleted lungs: Agreement between bedside techniques and CT imaging. BMC Anesthesiol 2014; 14:64. 17. Frerichs I, Hinz J, Herrmann P, et al. Detection of local lung air content by electrical impedance tomography compared with electron beam CT. J Appl Physiol 2002; 93:660–666. 18. Yoshida T, Torsani V, Gomes S, et al. Spontaneous effort causes occult pendelluft during mechanical ventilation. Am J Respir Crit Care Med 2013; 188:1420–1427. 19. van der Burg PS, Miedema M, de Jongh FH, et al. Cross-sectional changes in lung volume measured by electrical impedance tomography are representative for the whole lung in ventilated preterm infants. Crit Care Med 2014; 42:1524–1530. 20. Hinz J, Hahn G, Neumann P, et al. End-expiratory lung impedance change enables bedside monitoring of end-expiratory lung volume change. Intensive Care Med 2003; 29:37–43. 21. Meier T, Luepschen H, Karsten J, et al. Assessment of regional lung recruitment and derecruitment during a PEEP trial based on electrical impedance tomography. Intensive Care Med 2008; 34:543–550. 22. Bikker IG, Leonhardt S, Bakker J, Gommers D. Lung volume calculated from electrical impedance tomography in icu patients at different peep levels. Intensive Care Med 2009; 35:1362–1367. 23. Karsten J, Meier T, Iblher P, et al. The suitability of EIT to estimate EELV in a clinical trial compared to oxygen wash-in/wash-out technique. Biomedizinische Technik Biomedical Engin 2014; 59:59–64. 24. Cornejo RA, Diaz JC, Tobar EA, et al. Effects of prone positioning on lung && protection in patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2013; 188:440–448. This study investigated the effect of prone position on the different volumes (hyperinflated, normally aerated and poorly or non aerated) as estimated by CT scan in ARDS patients, as well as the protective effect on tidal recruitment. 25. Dellamonica J, Lerolle N, Sargentini C, et al. Effect of different seated & positions on lung volume and oxygenation in acute respiratory distress syndrome. Intensive Care Med 2013; 39:1121–1127. This physiological study indicated significant increase in EELV and decrease in strain during verticalization. 26. Razazi K, Thille AW, Carteaux G, et al. Effects of pleural effusion drainage on oxygenation, respiratory mechanics, and hemodynamics in mechanically ventilated patients. Annals Am Thor Soc 2014; 11:1018–1024. 27. Chiumello D, Marino A, Cressoni M, et al. Pleural effusion in patients with acute lung injury: a CT scan study. Crit Care Med 2013; 41:935–944. 28. Cortes-Puentes GA, Cortes-Puentes LA, Adams AB, et al. Experimental intra-abdominal hypertension influences airway pressure limits for lung protective mechanical ventilation. J Trauma Acute Care Surg 2013; 74:1468– 1473. 29. Regli A, Chakera J, De Keulenaer BL, et al. Matching positive end-expiratory pressure to intra-abdominal pressure prevents end-expiratory lung volume decline in a pig model of intra-abdominal hypertension. Crit Care Med 2012; 40:1879–1886. 30. Nakahashi S, Gando S, Ishikawa T, et al. Effectiveness of end-expiratory lung volume measurements during the lung recruitment maneuver for patients with atelectasis. J Crit Care 2013; 28:534.e1-5. 31. Liu Q, Li W, Zeng QS, et al. Lung stress and strain during mechanical ventilation in animals with and without pulmonary acute respiratory distress syndrome. J Surg Res 2013; 181:300–307. 32. Gonzalez-Lopez A, Garcia-Prieto E, Batalla-Solis E, et al. Lung strain and biological response in mechanically ventilated patients. Intensive Care Med 2012; 38:240–247. &
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