Lung ultrasound in the critically ill

Purpose of reviewLung ultrasound, which allows a bedside visualization of the lungs, is increasingly used in critical care. This review aims at highlighting a simple approach to this new discipline. Recent findingsThe 10 basic signs are the bat sign (indicating pleural line), lung sliding (yielding the seashore sign), the A line (horizontal artifact), the quad and sinusoid sign indicating pleural effusion regardless of its echogenicity, the tissue-like and shred sign indicating lung consolidation, the B line and lung rockets (artifacts indicating interstitial syndrome), abolished lung sliding with the stratosphere sign, suggesting pneumothorax, and the lung point, indicating pneumothorax. All these disorders were assessed using computed tomography (CT) as a gold standard with sensitivity and specificity ranging from 90 to 100%, allowing us to consider ultrasound as a reasonable bedside gold standard in the critically ill. We use a simple gray-scale unit (without Doppler) with a microconvex probe. SummaryLung ultrasound can be used for diagnosing acute respiratory failure (BLUE protocol), managing acute circulatory failure (Fluid Administration Limited by Lung Sonography protocol), and decreasing the use of radiograph or CT (the Lung Ultrasound in the Critically Ill Favoring Limitation of Radiation project). This can be extended from sophisticated ICUs to more austere settings, from neonates to bariatric adults without adaptation, trauma and several other disciplines (anesthesiology, emergency medicine, pulmonology, etc.). Video abstracthttp://links.lww.com/COCC/A8.


INTRODUCTION
The lung is, with the heart, the main vital organ. The usual tools for its assessment in critical conditions are not perfect: physical examination (insufficient for fine diagnoses), bedside radiography (of limited accuracy), and even computed tomography (CT; risk of transportation, irradiation, and cost). Ultrasound is an old tool [1]. Its use in critical care, which began with the heart [2], was long confined to this area and, of course, did not consider lung in its scope [3,4]. However, a whole-body use of critical ultrasound was long proposed [5]. Intensivists, who would appreciate to find again the advantages of ultrasound (real time, noninvasive, bedside method, low cost, etc.) at the lung area, will have an optimal tool for answering most questions regarding the critically injured lung. Standardized signatures allow to diagnose and quantify not only pleural effusions, but also alveolar syndrome, interstitial syndrome, pneumothorax, including them for the diagnosis of an acute respiratory failure (BLUE protocol), and more, with accuracy near to CT.
Lung ultrasound is rather simple but must be methodologically learned. The lung is the most voluminous organ, but standardized points can simplify its analysis ( Fig. 1) [6]: the BLUE points [7]. For locating the lung surface, the longitudinal approach has the advantages of locating the pleural line in all circumstances (agitated, bariatric patients, subcutaneous emphysema, etc.). The patient's positioning must be specified because gravity locates fluids at dependent areas and gas at nondependent areas. Only short probes can be positioned at the back of supine, ventilated patients, as perpendicular as possible pointing to the sky and be at the best site.
Ten signs arising from the pleural line allow the mastery of the BLUE protocol, and only two for defining the normal lung surface (Fig. 2) [6]. The pleural line, located between two ribs and yielding the bat sign, indicates the parietal (and usually visceral) pleura. Lung sliding is a sparkling at the pleural line, yielding in M-mode the seashore sign. The A lines are horizontal artifactual repetitions of the pleural line displayed at regular intervals. The second main artifact, the B line, developed below, can be seen in normal individuals in some standardized areas.
Fluid pleural effusion, a familiar diagnosis [1,8], seems only recently 'discovered' by the intensive care world. In the BLUE protocol, pleural effusions, even minute, can have high relevance. We do not use the traditional criteria, which work only when the effusion is anechoic. We use instead the quad sign, indicating that the lung line (visceral pleura) is seen, roughly parallel to the pleural line (making a quad with rib shadows), and the sinusoid sign, indicating the inspiratory excursion of the lung line toward the pleural line ( Fig. 3) [6]. Both signs provide valuable accuracy (Table 1) [9][10][11][12][13][14]. The sinusoid sign indicates that fine-needle caliper can be used. Criteria allow safe needle insertion even in ventilated patients, even if radioccult effusion, provided a 15-mm safety distance is present [9]. We do not use ultrasound during thoracentesis.
Lung consolidation is a basic application (Fig. 3). We use two signs which prove quite specific [10]. The shred sign (indicating a shredded boundary between consolidated and aerated lung) is specific to nontranslobar consolidations. Translobar consolidations yield the quasi-specific tissue-like sign. The air bronchogram, rather specific, is redundant when it is seen inside a specific pattern (Table 1). It can be dynamic (dynamic air bronchogram) or static, helping for distinguishing nonretractile (pneumonia) from retractile (atelectasis) consolidations [15]. The BLUE protocol distinguishes whether a

KEY POINTS
Lung ultrasound is at best performed using simple grayscale units and certain microconvex probes (but any machine and any probe can work more or less).
All acute disorders can be assessed using standardized signatures and standardized areas of investigation (pleural effusion, lung consolidation, interstitial syndrome, pneumothorax, etc.), allowing immediate diagnosis, mastery of extreme settings (cardiac arrest), and decrease of radiations.
The BLUE protocol is an approach using lung and venous ultrasound for diagnosing the main causes of acute respiratory failure (pneumonia, pulmonary edema, COPD, asthma, pulmonary embolism, and pneumothorax).
Under fluid therapy, an interstitial syndrome can be generated on ultrasound at an early, clinically silent step, generating a change from A lines to B lines, providing a direct parameter of clinical volemia (principle of the FALLS protocol).
The impact of lung ultrasound in critical care can be extended without adaptation to all disciplines dealing at any degree with the lung (anesthesiology, cardiology, emergency medicine, nephrology, internal medicine, neurology, obstetrics, pediatrics, pulmonology, radiology, thoracic surgery, ultrasound, and even veterinarian fields). consolidation contains transudate (pulmonary edema), exudate (pneumonia and ARDS (adult respiratory distress syndrome) ), or blood (pulmonary embolism) [16 & ]. Interstitial syndrome, published 20 years ago, is central to the BLUE protocol [11,17]. One must accept abstract thinking, that is, using the language of artifacts. Pulmonary interstitial edema is designed by diffuse lung rockets (Table 1). Lung rockets are defined as at least three B lines between two ribs. The B line is an artifact with seven criteria (the first three constant and the four last quite constant): comet-tail, arising from the pleural line, moving with lung sliding, well defined, long, hyperechoic, and erasing A lines (Fig. 4). Many comet tails without clinical relevance are excluded by this definition [see BLUE protocol and Fluid Administration Limited by Lung Sonography (FALLS) protocol for the clinical relevance]. Note meanwhile that no routine test can detect interstitial syndrome easily (auscultation, bedside radiography, etc.). Counting the lung rockets allows us to differentiate subpleural interlobular thickening from ground-glass areas [11].
Pneumothorax is a daily concern (extreme emergency such as cardiac arrest, routine in ventilated patients, and thoracic procedures). This is in our opinion, as opposed to some experts [18 & ] a fully accessible application, provided one accepts to think sequentially (Fig. 5). Pneumothorax is sought for at standardized anterior points [7]. We first detect abolished lung sliding, a step far from specific (pleural symphysis, lung fibrosis, and abolition of lung compliance are some common causes). M-mode yields the standardized stratosphere sign. Lung sliding allows pneumothorax to be ruled out [19]. When lung sliding is abolished, the A-line sign (a negative search for B lines) defines, in the BLUE protocol, the A 0 profile. One B-line (even motionless) rules out pneumothorax [13]. The A 0 profile suggests pneumothorax. Then, a pathognomonic sign is sought for, the lung point [12]. This is a point where, the probe standstill at the supposed junction between pneumothorax and lung, sudden lung signs appear, usually on inspiration (lung sliding and lung rockets). This sign allows confident and quiet chest tube insertion. The lung point shows that ultrasound is a highly sensitive real-time method and allows us to assess the volume of the pneumothorax, including radioccult cases [14], to monitor untreated cases.   Space lacks for applications such as lung abscess, diaphragmatic function [20], the lung pulse for diagnosing atelectasis [21], and others.

CLINICAL APPLICATIONS USEFUL FOR THE INTENSIVIST
Here are some practical uses of lung ultrasound in the critically ill.

The BLUE protocol
At first sight, using ultrasound in acutely dyspneic patients may mean a loss of time. On the contrary, lung ultrasound allows us to approach the diagnosis before any test. Briefly, the BLUE protocol uses lung and venous ultrasound for drawing profiles [16 & ]. It is devoted to earlier diagnosis, mainly meaning quicker relief of these suffering patients. All we need is a simple machine, our multipurpose microconvex probe, and the analysis, at the standardized BLUE points, of some items: lung sliding, lung rockets, and posterolateral alveolar and pleural syndrome (called PLAPS). Combined together, allocated to certain locations, they originate seven profiles (Fig. 6).
(1) The A profile, combining lung sliding and A lines at the anterior wall, defines the normal lung surface.  (2) The B profile associates anterior lung sliding and lung rockets. The association of A profile with venous thrombosis favors the diagnosis of pulmonary embolism, with 81% sensitivity and 99% specificity. The B profile suggests the diagnosis of hemodynamic pulmonary edema, with 97% sensitivity and 95% specificity. The A 0 profile strongly suggests pneumothorax, its association with a lung point indicates pneumothorax. Regarding pneumonia, due to a substantial number of possible germs, four profiles have been observed: the B 0 profile, the C profile, the A/B profile, and the A-V-PLAPS profile.
These profiles have all in all an 89% sensitivity and 94% specificity. The nude profile in a few words defines normal lungs and normal veins, and is associated to acute exacerbation of chronic obstructive pulmonary disease or asthma; if the auscultation did not show wheezing, and in the case of any suspicion, the search for pulmonary embolism (without deep venous thrombosis) is necessary, schematically. Each profile is explained by the pathophysiology (e.g., the exudative process of pneumonia sticks the lung to the wall, generating the B 0 profile).
A simplified echocardiography (real time without Doppler) is associated with the BLUE protocol, usually redundant. In case of discordance, note that the BLUE protocol provides a direct approach to the suffering organ (the lung).
The BLUE protocol can be adapted to multiple settings: the trauma [22], the neonate [23][24][25], and ARDS. In ARDS, lung recruitment is a usual concern [26]. Ultrasound can be of help for measuring lung recruitment [27]. Several points cannot be dealt with, including the case of the rare diagnoses, the patients with several diagnoses, apparent and true limitations (all answered in [6]). The characteristics of lung rockets (distribution and dynamics) help in the distinction between hemodynamic pulmonary edema and ARDS.

The Fluid Administration Limited by Lung Sonography protocol
Lung artifacts will now be used for answering two basic questions raised in acute circulatory failure. Who will benefit from fluid therapy? If administered, when to stop fluid? This approach is based upon the concept that ultrasound interstitial syndrome is an indicator of pulmonary artery occlusion pressure [28].
The FALLS protocol sequentially follows Weil's classification of shocks for a fast diagnosis [29 & ]. It initiates the investigation by a simple cardiac sonography, searching for substantial pericardial fluid or enlarged right ventricle, then for an A 0 profile (BLUE protocol). This rules out pericardial tamponade, pulmonary embolism, and pneumothorax, that is, obstructive shock. If the BLUE protocol does not show a B profile, pulmonary edema can be ruled out, that is, schematically, left cardiogenic shock. Patients who display an A profile are called FALLS responders: they will benefit from fluid therapy. They are rapidly treated, as both the remaining causes, hypovolemic and distributive shock schematically, require fluids. The hypovolemic shock is defined by an improvement of circulatory parameters after fluid therapy. If these parameters do not improve, fluid therapy is resumed, eventually generating a fluid overload, which, in this sequence, will rapidly show up the only remaining cause, that is, distributive shock, which in current practice is, schematically, septic shock. Briefly, among several advantages, the FALLS protocol provides a direct parameter of clinical volemia with an on and off effect. More than lung water, it measures an earlier parameter: lung interstitial water. Usual tools can be associated in parallel. Familiar guidelines (early and massive fluid therapy in sepsis) are followed [30], with the advantage of earlier therapy, discontinued on the basis of a pathophysiological phenomenon. The FALLS protocol remains open to any criticism.

Cardiac arrest and lung ultrasound
In a few words, as the role of ultrasound in cardiac arrest is to rapidly find a reversible cause, SESAME protocol (the first half of Sequential Echographic Screening Assessing Mechanism Or Origin of Shock of Indistinct Cause) begins with the lung: pneumothorax is a frequent reversible cause, lung windows are quite always available (unlike cardiac windows), and the A profile or A 0 profile are identified within seconds, thus justifying this priority.

The Lung Ultrasound in the Critically Ill Favoring Limitation of Radiation project
Medical irradiation is deleterious [31,32,33 & ]. The bedside radiography can be misleading [34,35].
Lung Ultrasound in the Critically Ill Favoring Limitation of Radiation (LUCI-FLR) is one of our main targets [6,35]. The overall accuracy of ultrasound holds between 90 and 100% when compared with CT (Table 1), making this project legitimate. The economy of radiations can be huge, yet the physician should care at not eradicating radiography (the idea, as well as the acronym, would be unsuitable). A reasonable target of the LUCI-FLR project is to decrease, in the next 30 years, one-third of radiographs and two-thirds of CTs. It is based on the proven fact that ultrasound accuracy is superior to radiography, and quite equal to CT, if not superior in some cases [36]. Mastering lung ultrasound, the physician will gradually be familiar with the LUCI-FLR project. We can highlight just one standardized application: each time one checks for the absence of pneumothorax, a view showing seashore sign allows avoiding the traditional (and not sensitive) radiograph.

OTHER CONSIDERATIONS, FROM TRAINING TO CLINICAL APPLICATIONS
An exponential number of articles confirm the reality of lung ultrasound. We can cite just a very few [18 & ,20,23,27,37-69,70 & ]. The training should be the least issue. A teaching from the recognized centers, using standardized signs, standardized technique, and the use of simple but efficient machines, warrants for a steep learning curve [10,35,71]. Lung ultrasound is not really 'ultrasound' (this expert discipline) for several reasons, among which only two signs describe the normal lung surface, wherever the probe is applied. B lines will be distinguished from Z lines and E lines using standardized criteria, etc.
For taking the best of lung ultrasound, we advise to change softly: this tool may impact the habits so deeply that it may appear wise to do quietly, step by step, with always a hand on the traditional tools. The target of the LUCI-FLR project is to limit, not eradicate, radiations. There will always be situations in which radiograph or CT will be indicated, and our traditional culture used.
Lung ultrasound is a new tool which provides real-time, dynamic signs, such as lung sliding, dynamic air bronchogram, and lung pulse, which cannot be obtained using other tools: lung sliding, for example, is an indicator of lung compliance.

WHICH EQUIPMENT?
This is not, and this is, a critical point. Modern laptop machines with their usual three and four probes are good, any kind of machine is able to scan the lung, more or less. We just inform that the tool we use since 1992 is better in all aspects: smaller in the width dimension (the only important one) than the current laptops with a 30-cm width, faster (7 s), cleaner with its flat keyboard, more universal with a unique probe (see below), and much cheaper. The keyboard is devoid of many functions which not only can confuse, but also sometimes spoil the image, such as harmonics and time lag filters among many details. As we permanently use two hands in critical ultrasound, pocket machines are not a critical advantage in hospitals (in airborne medicine, it is). Our system uses a microconvex probe, which, unlike some other microconvex probes (high resolution and depth up to 17 or 25 cm), is a perfect compromise allowing immediate whole-body analysis (including heart, veins, and belly). Our protocol in cardiac arrest (SESAME protocol) is the best example showing that all these details interact with each other for an optimal management, the very definition of holistic ultrasound.

FEW LIMITATIONS
A feature of lung ultrasound (in the critically ill) is a poor number of real limitations, schematically, huge subcutaneous emphysema, dressings, and corsets. Exceptionally, scannings are difficult: usually, the signs are accessible and standardized. Lung windows are quite always accessible: air (the main hindrance for cardiac and abdominal echography) is specifically on focus. Deep disorders are not accessible, but their detection does not change the immediate therapy (lymph nodes, etc.). The anterior analysis of bariatric patients is usually simple, whereas the posterior ones more difficult.

CONCLUSION
In conclusion, one may ask, with so clear and multiple advantages, why was this method neglected or worse, denied, for so many decades. More pragmatically, we will raise the question on how. How to give an optimal culture (based upon simplicity) to the physicians, enabling vital diagnoses with a step ahead compared with any other technique, this was approached in this review. Some benefits will be measured (lives saved, duration of stay, etc.), but the main one is available now: increased patient's comfort. We like to remind that ultrasound is a genuine stethoscope (scope -instrument to observe and stethos -the thorax): a visual medicine. Critical ultrasound recently made a substantial change in modern medicine, but if the lung is now added, one can just imagine how this inclusion will impact this new discipline [72].

Conflicts of interest
The author has no conflicts of interest to declare. Videos of the main profiles of the BLUE protocol are available at www.CEURF.net, section BLUE protocol.

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