International Journal of Critical Illness and Injury Science

MINI REVIEW
Year
: 2019  |  Volume : 9  |  Issue : 1  |  Page : 11--15

Usefulness of ultrasound in the management of acute respiratory distress syndrome


Anis Chaari, Kamel Bousselmi, Walid Assar, Vaguish Kumar, Elsayed Khalil, Vipin Kauts, Karim Abdelhakim 
 Department of Critical Care, King Hamad University Hospital, Al Muharaq, Kingdom of Bahrain

Correspondence Address:
Dr. Anis Chaari
Department of Critical Care, King Hamad University Hospital, Building 234, Road 2835, Block 228, Bussaiteen, PO Box: 24343, Al Muharaq
Kingdom of Bahrain

Abstract

Acute respiratory distress syndrome (ARDS) is a life-threatening disease. Different imaging techniques have been used to diagnose and guide the ventilatory management of patients with ARDS. Chest ultrasound is a reliable tool to identify interstitial syndrome, lung consolidation, lung collapse, and pleural effusion. In addition, echocardiography is essential in the diagnosis of diastolic left ventricle dysfunction and the estimation of elevated ventricle filling pressures, which is necessary before diagnosing ARDS. Therefore, combining chest and heart ultrasound assessment is useful to diagnose ARDS and guide the ventilatory management of the disease. Available data in the literature suggest that protocol-based approaches should be implemented for the purposes of diagnosis and management.



How to cite this article:
Chaari A, Bousselmi K, Assar W, Kumar V, Khalil E, Kauts V, Abdelhakim K. Usefulness of ultrasound in the management of acute respiratory distress syndrome.Int J Crit Illn Inj Sci 2019;9:11-15


How to cite this URL:
Chaari A, Bousselmi K, Assar W, Kumar V, Khalil E, Kauts V, Abdelhakim K. Usefulness of ultrasound in the management of acute respiratory distress syndrome. Int J Crit Illn Inj Sci [serial online] 2019 [cited 2019 May 23 ];9:11-15
Available from: http://www.ijciis.org/text.asp?2019/9/1/11/253758


Full Text



 Introduction



Acute respiratory distress syndrome (ARDS) was first reported by Ashbaugh et al. as a life-threatening, severe, and refractory hypoxemia related to an acute alveolar and capillary damage.[1] Its incidence ranges between 4.2 and 58 cases per 100,000 persons/year.[2],[3],[4] The ARDS-related mortality is high and is reported from 36% to 44%.[3],[5] Therefore, the definition of ARDS has been regularly updated in order to improve and standardize the ventilatory and nonventilatory management.[6],[7] Common components of these different definitions include bilateral alveolar infiltrates that cannot be exclusively explained by either left ventricle dysfunction or fluid overload.[6],[7] Therefore, lung and cardiac imaging is important to establish the diagnosis of ARDS and, possibly, in evaluating the response to treatment. During the last few decades, chest X-ray and computed tomography (CT) of the chest have been widely used in patients with ARDS.[8] Even though bedside chest X-ray is part of the diagnostic criteria for ARDS, several limitations exist.[8],[9],[10],[11] On the other hand, performing a CT chest requires moving the patient and is risky in severely hypoxemic patients.[10],[12] CT has been shown to be useful in identifying the distribution of the alveolar damage, assessing positive end-expiratory pressure (PEEP)-induced alveolar recruitment, and recognizing ventilator-induced lung injury.[8],[12],[13],[14]

Ultrasonography techniques are being increasingly used in the intensive care units (ICUs).[15] These techniques are noninvasive and can be easily performed at the bedside. The current review addresses the usefulness of the technique for the management of patients with ARDS.

Diagnosis of acute respiratory distress syndrome

The definition of ARDS has been updated in 2012.[6] Accordingly, the diagnosis of ARDS is based on clinical, radiological, and oxygenation criteria. The imaging criteria consist of bilateral opacities, not fully explained by effusion, lobar/lung collapse, or nodules.[6] The ultrasound findings are closely correlated to the usual evolution of ARDS. In fact, the hallmark of the 1st week following pulmonary or extrapulmonary insult is the occupation of interstitial and alveolar space by protein-rich fluid.[12] The proliferative phase follows the exudative phase and starts at the 2nd week with stabilization of the imaging findings. Starting from the 3rd week, the lungs evolve toward either fibrosis or resolution of the ARDS.[4],[12] Therefore, at the stage of interstitial syndrome with moderate aeration loss, lung ultrasound (LUS) shows vertical well-defined spacing lines starting from the pleural line and reaching the edge of the screen. These B1 lines reflect the thickening of the interlobular septa.[8],[11],[16],[17] In patients with significant aeration loss, these B lines become coalescent and are therefore labeled as B2 lines.[8],[11],[16],[17] Finally, lung consolidations with significant aeration loss appear as poorly defined hypoechoic areas, in which hyperechoic lines or pinpoint images related to air bronchogram can be identified.[8],[11],[16],[17] Heterogeneity is the hallmark of imaging abnormalities in ARDS.[10],[12] Therefore, these abnormalities should be screened bilaterally in 12 areas as previously described.[11],[18] Moreover, LUS has been shown to be useful to predict the onset of ARDS in several categories of patients such as those with chest trauma.[19]

The main differential diagnosis of ARDS is cardiogenic pulmonary edema. Several studies highlighted that LUS may be useful to make the distinction between these two conditions. In a prospective study including 58 patients (40 patients with pulmonary edema and 18 patients with acute lung injury or ARDS), Copetti et al.[20] reported that alveolo-interstitial syndrome was found in all cases. However, pleural-line abnormalities, consolidation, spared lung areas, pleural effusion, and lung pulse sign were significantly more common in patients with noncardiogenic pulmonary edema.

Making the difference between acute respiratory syndrome and cardiogenic pulmonary edema based on LUS only is challenging. In fact, several studies mainly conducted in emergency departments suggest that most of the patients presenting with acute respiratory failure with B lines identified by LUS are diagnosed as cardiogenic pulmonary edema.[21],[22] In a prospective study conducted in a prehospital setting, Laursen et al.[23] reported that in patients with acute respiratory failure, the identification of B lines had a sensitivity of 94.4% and a specificity of 77.3% to predict cardiogenic pulmonary edema. Therefore, several patients with ARDS and showing B lines on chest ultrasound might be mistakenly diagnosed as pulmonary edema. Therefore, combining LUS findings with echocardiography has been reported to be more useful in this regard. In fact, echocardiography is a useful tool to assess left ventricular diastolic function and left ventricular filling pressure and therefore can rule out elevated pulmonary artery occlusion pressure.[24],[25] In a prospective study including 134 patients with hypoxemic acute respiratory failure, Sekiguchi et al.[26] reported that moderate-to-severe left ventricle function impairment, a minimal inferior vena cava diameter above 23 mm, and left-sided pleural effusion are in favor of cardiogenic pulmonary edema rather than ARDS in patients with bilateral B lines. In the group of patients with diastolic function assessment, the authors reported that ARDS is more likely in patients with E/e' ratio ≤8.3.

Ultrasound and ventilator management

Lung protective strategies have been shown to be associated with improved outcome and less complications in patients with ARDS.[27] Accordingly, low tidal volume should be delivered to all patients and high PEEP should be applied in patients with moderate-to-severe ARDS.[6] Prone position should be attempted in patients with severe ARDS.[6] The selection of the best level of PEEP has been challenging. Several studies have suggested that the level of PEEP might be adjusted according to the oxygenation parameters,[28],[29] whereas others suggested that it should be based on lung mechanics (lung compliance, plateau pressure, pressure–volume curve, and stress index).[30],[31],[32],[33] Imaging techniques, mainly chest CT, were also used to assess the effect of increasing the PEEP level on alveolar recruitment or overdistension.[10],[13],[34] In the last decade, LUS has become a seductive method that can be taken as a surrogate of CT in this regard.[35] In a prospective study including thirty patients with ARDS and ten patients with acute lung injury, Bouhemad et al.[16] reported that LUS can be a useful tool to assess lung aeration after increasing PEEP level. Moreover, the assessment of the anterior, lateral, and posterior lung areas showed that the benefit from PEEP was mainly observed in the lower part of the anterior and lateral lungs as well as the upper and posterior part of the lungs. Total or partial reaeration of the consolidated lung was seldom observed and was more likely to occur in the lower parts of the lungs. Similarly, Rode et al.[36] reported a significant positive correlation between the required PEEP to recruit subpleural consolidation and the lower inflection point identified on the pressure–volume curve. A significant correlation between the lung reaeration assessed by LUS and oxygen partial pressure has been also reported.[37]

The improvement of lung aeration can also be achieved by recruitment maneuvers. Recent data suggest that LUS can be helpful to evaluate the effect of these maneuvers. In an experimental study, Li et al.[38] reported that ultrasound-guided recruitment maneuver strategy results in significant improvement of lung reaeration when compared to oxygenation-guided strategy.

Ultrasound and hemodynamic management

Applying a high level of PEEP is a cornerstone of the open-lung ventilation strategy that has been shown to be associated with a significant decrease of in-hospital and ICU mortality.[39] However, one of the major drawbacks of high PEEP levels is right ventricular dysfunction.[40],[41],[42],[43],[44] The incidence of acute cor pulmonale in patients with ARDS ranges between 20% and 25%.[42],[43],[45] Mekontso Dessap et al.[43] reported that predictive factors of cor pulmonale onset are pneumonia as a cause of ARDS, PaO2/FiO2 ratio below 150 mmHg, PaCO2 ≥48 mmHg, and a driving pressure ≥18 mmHg. Patients with right ventricular dysfunction have been reported to be prone to hemodynamic instability and are likely to require vasopressor support.[45] However, only severe cor pulmonale defined as right ventricular end-diastolic area by left ventricular end-diastolic area ratio above 1 has been reported to be associated with significant increase in mortality.[43] The echocardiographic findings can be also useful to predict the prognosis of patients with ARDS. In fact, Wadia et al.[46] reported a significant decrease of the tricuspid annular plane systolic excursion (TAPSE) in patients with ARDS. Moreover, the authors reported that the TAPSE was significantly correlated with altered oxygenation and was significantly lower in nonsurvivors. Therefore, it has been hypothesized that right ventricle assessment should be routinely performed in ARDS patients.[47],[48],[49] However, the available guidelines do not support the selection of PEEP level according to its effect on the right ventricle.[6]

Fluid management in patients with ARDS is challenging. Based on the results of a large randomized controlled trial, it has been shown that conservative fluid management is associated with significant increase of ventilator-free days.[50] However, applying a strict conservative fluid management is usually difficult in patients with ARDS and hypovolemic status. In fact, one previous experimental study has shown that recruitment maneuver in hypovolemic pigs was associated with a significant decrease in the left end ventricular volume as well as the cardiac output. This negative effect was counterbalanced by improving the volemic status.[51] Similarly, implementing this strategy in patients with septic shock who always require fluid resuscitation is challenging. In this regard, by using LUS, Caltabeloti et al.[52] assessed the effect of fluid loading in patients with moderate-to-severe ARDS associated with septic shock in 36 patients. The authors reported a persistent worsening of the lung aeration despite transient improvement of the cardiac output and the oxygenation parameters. Therefore, bedside ultrasound assessment is a useful technique to assess the effect of fluid resuscitation on both hemodynamic status and lung condition, especially in a selected group of patients. In fact, the re-analysis of large randomized controlled trials data showed that the following two subphenotypes of ARDS can be identified: subphenotype 1 characterized by mild inflammatory response, in which mortality can be reduced with liberal fluid resuscitation, and subphenotype 2 characterized by increased inflammatory markers (interleukin 8, interleukin 6, and tumor necrosis factor r1), acidosis, shock, and vasopressor requirement, in which liberal fluid resuscitation is potentially harmful and associated with significant worsening of the outcome.[28],[53],[54] Whether echocardiographic and LUS studies can be helpful to differentiate these two subphenotypes needs to be investigated.

Protocoled approach for acute respiratory distress syndrome

During the last few decades, protocoled sonography approaches have been established to improve ultrasound-based diagnostic strategies.[55] The Bedside Lung Ultrasound in Emergency protocol has been elaborated to get an ultrasound-based systematic approach in patients admitted to the emergency departments with acute respiratory failure.[56] The protocol includes different profiles including the B profile suggesting pulmonary edema.[55],[56] However, it does not provide enough criteria to make the difference between cardiogenic pulmonary edema and acute respiratory distress. Fluid Administration Limited by Lung Sonography protocol has been developed to add more details about basic echocardiography findings and to guide fluid resuscitation therapy accordingly.[55] Similarly, there are no specific recommendations for the diagnosis of ARDS. Based on the Berlin definition of ARDS, combining clinical and imaging findings could be the best option in patients with hypoxemic acute respiratory failure. Therefore, the combination of LUS findings suggesting pulmonary edema with echocardiographic findings ruling out left ventricular dysfunction and increased left ventricular filling pressure could be useful to diagnose ARDS.

 Conclusion



Ultrasound techniques are noninvasive and reproducible imaging tools that can be performed at the bedside. Currently available data in the literature suggest that these techniques are useful in patients with ARDS as they can help to establish the diagnosis, to optimize the ventilation settings, and to avoid hemodynamic compromise. Combining LUS and echocardiography is more helpful for the management of patients with acute respiratory syndrome.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet 1967;2:319-23.
2Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, et al. Incidence and outcomes of acute lung injury. N Engl J Med 2005;353:1685-93.
3Dushianthan A, Grocott MP, Postle AD, Cusack R. Acute respiratory distress syndrome and acute lung injury. Postgrad Med J 2011;87:612-22.
4Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-49.
5Phua J, Badia JR, Adhikari NK, Friedrich JO, Fowler RA, Singh JM, et al. Has mortality from acute respiratory distress syndrome decreased over time?: A systematic review. Am J Respir Crit Care Med 2009;179:220-7.
6Ferguson ND, Fan E, Camporota L, Antonelli M, Anzueto A, Beale R, et al. The berlin definition of ARDS: An expanded rationale, justification, and supplementary material. Intensive Care Med 2012;38:1573-82.
7Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, et al. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 1994;149:818-24.
8Arbelot C, Ferrari F, Bouhemad B, Rouby JJ. Lung ultrasound in acute respiratory distress syndrome and acute lung injury. Curr Opin Crit Care 2008;14:70-4.
9Zompatori M, Ciccarese F, Fasano L. Overview of current lung imaging in acute respiratory distress syndrome. Eur Respir Rev 2014;23:519-30.
10Chiumello D, Froio S, Bouhemad B, Camporota L, Coppola S. Clinical review: Lung imaging in acute respiratory distress syndrome patients – An update. Crit Care 2013;17:243.
11Lichtenstein D, Goldstein I, Mourgeon E, Cluzel P, Grenier P, Rouby JJ, et al. Comparative diagnostic performances of auscultation, chest radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004;100:9-15.
12Sheard S, Rao P, Devaraj A. Imaging of acute respiratory distress syndrome. Respir Care 2012;57:607-12.
13Pesenti A, Musch G, Lichtenstein D, Mojoli F, Amato MB, Cinnella G, et al. Imaging in acute respiratory distress syndrome. Intensive Care Med 2016;42:686-98.
14Bouhemad B, Zhang M, Lu Q, Rouby JJ. Clinical review: Bedside lung ultrasound in critical care practice. Crit Care 2007;11:205.
15Gardelli G, Feletti F, Gamberini E, Bonarelli S, Nanni A, Mughetti M, et al. Using sonography to assess lung recruitment in patients with acute respiratory distress syndrome. Emerg Radiol 2009;16:219-21.
16Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby JJ, et al. Bedside ultrasound assessment of positive end-expiratory pressure-induced lung recruitment. Am J Respir Crit Care Med 2011;183:341-7.
17Lichtenstein D, Mezière G. A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: The comet-tail artifact. Intensive Care Med 1998;24:1331-4.
18Doerschug KC, Schmidt GA. Intensive care ultrasound: III. Lung and pleural ultrasound for the intensivist. Ann Am Thorac Soc 2013;10:708-12.
19Leblanc D, Bouvet C, Degiovanni F, Nedelcu C, Bouhours G, Rineau E, et al. Early lung ultrasonography predicts the occurrence of acute respiratory distress syndrome in blunt trauma patients. Intensive Care Med 2014;40:1468-74.
20Copetti R, Soldati G, Copetti P. Chest sonography: A useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome. Cardiovasc Ultrasound 2008;6:16.
21Pivetta E, Goffi A, Lupia E, Tizzani M, Porrino G, Ferreri E, et al. Lung ultrasound-implemented diagnosis of acute decompensated heart failure in the ED: A SIMEU multicenter study. Chest 2015;148:202-10.
22Laursen CB, Sloth E, Lassen AT, Christensen R, Lambrechtsen J, Madsen PH, et al. Point-of-care ultrasonography in patients admitted with respiratory symptoms: A single-blind, randomised controlled trial. Lancet Respir Med 2014;2:638-46.
23Laursen CB, Hänselmann A, Posth S, Mikkelsen S, Videbæk L, Berg H, et al. Prehospital lung ultrasound for the diagnosis of cardiogenic pulmonary oedema: A pilot study. Scand J Trauma Resusc Emerg Med 2016;24:96.
24Vignon P, Repessé X, Vieillard-Baron A, Maury E. Critical care ultrasonography in acute respiratory failure. Crit Care 2016;20:228.
25Boussuges A, Blanc P, Molenat F, Burnet H, Habib G, Sainty JM, et al. Evaluation of left ventricular filling pressure by transthoracic Doppler echocardiography in the Intensive Care Unit. Crit Care Med 2002;30:362-7.
26Sekiguchi H, Schenck LA, Horie R, Suzuki J, Lee EH, McMenomy BP, et al. Critical care ultrasonography differentiates ARDS, pulmonary edema, and other causes in the early course of acute hypoxemic respiratory failure. Chest 2015;148:912-8.
27Neto AS, Simonis FD, Barbas CS, Biehl M, Determann RM, Elmer J, et al. Lung-protective ventilation with low tidal volumes and the occurrence of pulmonary complications in patients without acute respiratory distress syndrome: A systematic review and individual patient data analysis. Crit Care Med 2015;43:2155-63.
28Brower RG, Lanken PN, MacIntyre N, Matthay MA, Morris A, Ancukiewicz M, et al. Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome. N Engl J Med 2004;351:327-36.
29Meade MO, Cook DJ, Griffith LE, Hand LE, Lapinsky SE, Stewart TE, et al. Astudy of the physiologic responses to a lung recruitment maneuver in acute lung injury and acute respiratory distress syndrome. Respir Care 2008;53:1441-9.
30Valentini R, Aquino-Esperanza J, Bonelli I, Maskin P, Setten M, Danze F, et al. Gas exchange and lung mechanics in patients with acute respiratory distress syndrome: Comparison of three different strategies of positive end expiratory pressure selection. J Crit Care 2015;30:334-40.
31Mercat A, Richard JC, Vielle B, Jaber S, Osman D, Diehl JL, et al. Positive end-expiratory pressure setting in adults with acute lung injury and acute respiratory distress syndrome: A randomized controlled trial. JAMA 2008;299:646-55.
32Chen L, Chen GQ, Shore K, Shklar O, Martins C, Devenyi B, et al. Implementing a bedside assessment of respiratory mechanics in patients with acute respiratory distress syndrome. Crit Care 2017;21:84.
33Chiumello D, Cressoni M, Carlesso E, Caspani ML, Marino A, Gallazzi E, et al. Bedside selection of positive end-expiratory pressure in mild, moderate, and severe acute respiratory distress syndrome. Crit Care Med 2014;42:252-64.
34Chiumello D, Marino A, Brioni M, Cigada I, Menga F, Colombo A, et al. Lung recruitment assessed by respiratory mechanics and computed tomography in patients with acute respiratory distress syndrome. What is the relationship? Am J Respir Crit Care Med 2016;193:1254-63.
35Lu Q. How to assess positive end-expiratory pressure-induced alveolar recruitment? Minerva Anestesiol 2013;79:83-91.
36Rode B, Vučić M, Siranović M, Horvat A, Krolo H, Kelečić M, et al. Positive end-expiratory pressure lung recruitment: Comparison between lower inflection point and ultrasound assessment. Wien Klin Wochenschr 2012;124:842-7.
37Stefanidis K, Dimopoulos S, Tripodaki ES, Vitzilaios K, Politis P, Piperopoulos P, et al. Lung sonography and recruitment in patients with early acute respiratory distress syndrome: A pilot study. Crit Care 2011;15:R185.
38Li DK, Liu DW, Long Y, Wang XT. Use of lung ultrasound to assess the efficacy of an alveolar recruitment maneuver in rabbits with acute respiratory distress syndrome. J Ultrasound Med 2015;34:2209-15.
39Lu J, Wang X, Chen M, Cheng L, Chen Q, Jiang H, et al. An open lung strategy in the management of acute respiratory distress syndrome: A systematic review and meta-analysis. Shock 2017;48:43-53.
40Jardin F, Gueret P, Dubourg O, Farcot JC, Margairaz A, Bourdarias JP, et al. Right ventricular volumes by thermodilution in the adult respiratory distress syndrome. A comparative study using two-dimensional echocardiography as a reference method. Chest 1985;88:34-9.
41Legras A, Caille A, Begot E, Lhéritier G, Lherm T, Mathonnet A, et al. Acute respiratory distress syndrome (ARDS)-associated acute cor pulmonale and patent foramen ovale: A multicenter noninvasive hemodynamic study. Crit Care 2015;19:174.
42Lhéritier G, Legras A, Caille A, Lherm T, Mathonnet A, Frat JP, et al. Prevalence and prognostic value of acute cor pulmonale and patent foramen ovale in ventilated patients with early acute respiratory distress syndrome: A multicenter study. Intensive Care Med 2013;39:1734-42.
43Mekontso Dessap A, Boissier F, Charron C, Bégot E, Repessé X, Legras A, et al. Acute cor pulmonale during protective ventilation for acute respiratory distress syndrome: Prevalence, predictors, and clinical impact. Intensive Care Med 2016;42:862-70.
44Gernoth C, Wagner G, Pelosi P, Luecke T. Respiratory and haemodynamic changes during decremental open lung positive end-expiratory pressure titration in patients with acute respiratory distress syndrome. Crit Care 2009;13:R59.
45Boissier F, Katsahian S, Razazi K, Thille AW, Roche-Campo F, Leon R, et al. Prevalence and prognosis of cor pulmonale during protective ventilation for acute respiratory distress syndrome. Intensive Care Med 2013;39:1725-33.
46Wadia SK, Shah TG, Hedstrom G, Kovach JA, Tandon R. Early detection of right ventricular dysfunction using transthoracic echocardiography in ARDS: A more objective approach. Echocardiography 2016;33:1874-9.
47Vieillard-Baron A, Price LC, Matthay MA. Acute cor pulmonale in ARDS. Intensive Care Med 2013;39:1836-8.
48Chiumello D, Pesenti A. The monitoring of acute cor pulmonale is still necessary in “Berlin” ARDS patients. Intensive Care Med 2013;39:1864-6.
49Bouferrache K, Vieillard-Baron A. Acute respiratory distress syndrome, mechanical ventilation, and right ventricular function. Curr Opin Crit Care 2011;17:30-5.
50National Heart, Lung, and Blood Institute Acute Respiratory Distress Syndrome (ARDS) Clinical Trials Network, Wiedemann HP, Wheeler AP, Bernard GR, Thompson BT, Hayden D, et al. Comparison of two fluid-management strategies in acute lung injury. N Engl J Med 2006;354:2564-75.
51Nielsen J, Nilsson M, Fredén F, Hultman J, Alström U, Kjaergaard J, et al. Central hemodynamics during lung recruitment maneuvers at hypovolemia, normovolemia and hypervolemia. A study by echocardiography and continuous pulmonary artery flow measurements in lung-injured pigs. Intensive Care Med 2006;32:585-94.
52Caltabeloti F, Monsel A, Arbelot C, Brisson H, Lu Q, Gu WJ, et al. Early fluid loading in acute respiratory distress syndrome with septic shock deteriorates lung aeration without impairing arterial oxygenation: A lung ultrasound observational study. Crit Care 2014;18:R91.
53Famous KR, Delucchi K, Ware LB, Kangelaris KN, Liu KD, Thompson BT, et al. Acute respiratory distress syndrome subphenotypes respond differently to randomized fluid management strategy. Am J Respir Crit Care Med 2017;195:331-8.
54Acute Respiratory Distress Syndrome Network, Brower RG, Matthay MA, Morris A, Schoenfeld D, Thompson BT, et al. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med 2000;342:1301-8.
55Lichtenstein DA. BLUE-protocol and FALLS-protocol: Two applications of lung ultrasound in the critically ill. Chest 2015;147:1659-70.
56Lichtenstein D. Lung ultrasound in acute respiratory failure an introduction to the BLUE-protocol. Minerva Anestesiol 2009;75:313-7.