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How I do it: Lung ultrasound
© Gargani and Volpicelli; licensee BioMed Central Ltd. 2014
Received: 26 April 2014
Accepted: 25 June 2014
Published: 4 July 2014
In the last 15 years, a new imaging application of sonography has emerged in the clinical arena: lung ultrasound (LUS). From its traditional assessment of pleural effusions and masses, LUS has moved towards the revolutionary approach of imaging the pulmonary parenchyma, mainly as a point-of-care technique. Although limited by the presence of air, LUS has proved to be useful in the evaluation of many different acute and chronic conditions, from cardiogenic pulmonary edema to acute lung injury, from pneumothorax to pneumonia, from interstitial lung disease to pulmonary infarctions and contusions. It is especially valuable since it is a relatively easy-to-learn application of ultrasound, less technically demanding than other sonographic examinations. It is quick to perform, portable, repeatable, non-ionizing, independent from specific acoustic windows, and therefore suitable for a meaningful evaluation in many different settings, both inpatient and outpatient, in both acute and chronic conditions.
In the next few years, point-of-care LUS is likely to become increasingly important in many different clinical settings, from the emergency department to the intensive care unit, from cardiology to pulmonology and nephrology wards.
What is lung ultrasound?
The acoustic limitations of ultrasound in the assessment of an air-rich organ such as the lung can paradoxically become a diagnostic advantage. In some conditions the presence of air between the chest wall and the lung parenchyma causes a decisive change of the dynamic characteristics of the sonographic artefact image of the lung described so far. In pneumothorax (PNX) lung sliding is always absent , since it can be observed if the lung and the parietal pleura are in direct apposition, but not when the physical acoustic enemy – the air – is between the two pleural layers. For similar reasons, no B-lines can be seen in the context of a PNX, since B-lines can be visualized only at an air-tissue acoustic interface, when the visceral pleura is opposing the parietal pleura. Another sign helps rule out PNX, the lung pulse, which refers to the subtle rhythmic movement of the lung upon the parietal pleura, synchronous with cardiac beats . Like the respiratory movement, this cardiac movement of the lung cannot be detected by ultrasound if air is present between the visceral and parietal pleura. An easy step-by-step sonographic algorithm has been proposed to diagnose/exclude PNX by LUS [3, 10].
In summary, LUS may be defined as a powerful diagnostic imaging technique for anomalies of the pleural space  and a reliable densitometer of the lung parenchyma . This definition of LUS includes both its virtues, which should be included in clinical practice, as it is often time-, cost- and potentially life-saving; as well as its limitations, which should never be forgotten for a correct use of this technique.
How I do it: the setting, the scanning technique, the probe
The diagnostic approach based on LUS can vary according to different settings and clinical situations, following the main principles of what is today known as “point-of-care ultrasound”. Maximum effectiveness of the method is obtained through a clinically-driven and focused assessment. If properly driven and correctly interpreted, some sonographic signs become highly accurate for diagnosing specific pulmonary conditions. For example, in a stable patient with acute spontaneous pleuritic pain, ultrasound examination will start from the painful chest area , focusing on signs of focal pleural and parenchymal abnormality. If the pain is caused by a pulmonary condition with involvement of the parietal pleura, this will be easily detected by LUS. Indeed, LUS is a surface imaging technique, highly sensitive in detecting pleural abnormalities. The clinical suspicion and pre-test probability will guide the diagnostic process to rule in or rule out with high accuracy several conditions, such as PNX, pleuritis, pneumonia, lung peripheral infarction . In this setting, a highly specific sign is the lung point, which represents the transition point between the typical sonographic pattern of PNX (absence of lung sliding and of B-lines) into the normal pattern of lung sliding, and depicts the physical limit of PNX as mapped on the chest wall . However, the lung point can be employed to detect the extension of PNX, but not its volume. Up-to-now, LUS is not recognized as a method to differentiate between large and small PNX.
If the main clinical suspicion is the possibility of a PNX, the LUS examination is started from the non-dependent zones for air collection, corresponding to the anterior-inferior chest in the supine patient. In this case, examining only one hot zone per side will help rule out PNX with high sensitivity both in the extreme emergencies and in stable patients. The hot zone examination will also be enough to confirm PNX in unstable/cardiac arrest patients . Only in stable patients will examination be extended to the lateral chest to confirm PNX.
The LUS examination can be performed using any commercially available 2-D scanner. Different transducers have been used, such as phased array (cardiac), convex (abdominal), microconvex, and linear (vascular) probes. Higher frequencies and macro probes are useful for the evaluation of the pleural line and subpleural space, so should be preferred for assessing PNX. Phased-array probes can be successfully employed to detect pleural effusion, thanks to low frequency and consequent ability to provide a deeper view of the chest. However, these latter probes have limitations in detecting PNX and when a detailed examination of the sub-pleural space is needed. The convex and microconvex probes are the most universally used, all-purpose probes for LUS, thanks to their intermediate frequency values, which allow a reasonable visualization of the pleural line and subpleural space, without losing the overview of the chest. B-lines can be detected by all these different probes, but again low frequency probes are probably the best for this application. Although the number of B-lines may be slightly different when using different probes in a specific chest site, the overall clinical picture does not change by changing the transducer . The possibility of easily assessing B-lines with any kind of transducer is one of the advantages of this technique, so no one should give up on scanning a patient just because the “ideal” probe is not available.
Portable machines and pocket-sized devices have also been proposed for assessing B-lines, as well as pleural effusion [33–35]. There is no need for a second harmonic or Doppler imaging mode, so even older ultrasound machines can be employed. Visualization of lung consolidations is possible with all probes as well. In the case of a small consolidation, a phased-array transducer may offer less detail, whereas a linear transducer would magnify it. In the case of large consolidations, a linear probe may be unsuitable for detecting the consolidations’ borders precisely, whereas convex and microconvex, and even the phased-array transducers, would be more appropriate. The depth should be tailored to the patient: very thick ribcages, large muscles and obese patients need greater depths, even to visualize the pleural line. Very thin patients and children may require less depth. Depth should also be adjusted to the target of our examination: if we are looking for PNX, the depth should be lower, in order to better visualize the pleural line and assess the presence or absence of the sliding sign. If we are looking for a free pleural effusion, the depth should be greater, for a better overview of the costo-phrenic angles. Normally the focus should be positioned at the pleural line level, but it should be moved deeper when our main target is less superficial.
How I do it: interpretation
Interpretation of LUS images is usually not very challenging. We must keep in mind that LUS is more affected by lack of specificity than lack of sensitivity. A LUS pattern showing absent lung sliding or multiple B-lines or a lung consolidation may be not enough to establish a specific diagnosis, since it can be linked to different pathologic conditions . Indeed, this limitation in specificity is a common feature of several diagnostic tools that we routinely interpret in daily clinical practice, from physical examination to EKG, from chest X-ray to more sophisticated instrumental findings. The power of these tools resides in the interpretation of signs when combined with each other at bedside, together with a consideration of the overall clinical picture. When all patient characteristics are taken into account, including history, symptoms, physical examination, setting, comorbidity, medications, etc., specificity can increase significantly. For example, in a patient with systemic sclerosis and without any known left heart conditions, presence of multiple B-lines is more probably related to pulmonary fibrosis than to extravascular lung water. On the other hand, presence of multiple diffuse bilateral B-lines in a patient with reduced cardiac function is more likely to be related to extravascular lung water than to fibrosis .
Additional information deriving from a bedside focused ultrasound evaluation of other organs may also be helpful. This approach has been recently described in patients with undifferentiated hypotension, where the integrated point-of-care multiorgan ultrasonography of the heart, inferior vena cava, lungs and abdomen significantly agreed with a final clinical diagnosis obtained by retrospective chart review . A multiorgan ultrasound approach including lung, heart and peripheral veins recently showed a better performance also for the diagnosis of pulmonary embolism than LUS alone [44, 45].
A controversial issue is quantification of B-lines. In critically ill patients the assessment can be qualitative, since the ultrasound finding of acute conditions is usually well defined and clear. For instance, in a critically ill patient with acute respiratory failure, if the underlying condition is cardiogenic pulmonary edema, the sonographic appearance of the lungs will be striking, with multiple diffuse bilateral B-lines to convey a picture of “sonographic white lung”. In these patients, B-lines can also be found in the least dependent zones, i.e. the anterior chest. On the contrary, finding a limited number of B-lines (even if bilateral) in a very symptomatic respiratory failure patient should lead to excluding the diagnosis of a cardiogenic origin of the actual condition. In non-critical patients, a more careful assessment and quantification of B-lines may be useful, especially for the follow-up. As highlighted above, a semi-quantification of B-lines has been proposed  and subsequently used in many papers from different research groups [19–25, 35, 47–50]. For clinical purposes, the final number of B-lines can be categorized ranging from mild to severe degrees, similar to what is done for most echocardiographic parameters. This counting approach can be imprecise when considering single scanning sites, but nevertheless provides a reliable overall LUS picture, allowing more accurate monitoring of patients, both in acute conditions - i.e., rapid changes after diuretic therapy or dialysis [21–23] – but also in stable outpatients . Moreover, this approach has shown good intraobserver and interobserver variability, consistently < 10% [22, 46, 51].
How I do it: pediatric patients
Lung ultrasound can be very useful in neonates and children. The advantage in this population is related to the small size of the chest, which allows an optimal, although still indirect, visualization of the lungs. All LUS signs and patterns described in the adult are alike in neonates and children, in both normal and pathological conditions . A number of studies have described the usefulness of LUS in the pediatric population, from transient tachypnea of the newborn  to respiratory distress syndrome , from bronchiolitis  to post-cardiac surgery lung complications  and anesthesia-induced atelectasis . In the pediatric patients LUS is especially valuable in detecting pneumonia, with a sensitivity even higher than that of chest X-ray [58–60]. Given the small size of a child’s chest, a linear probe allows the best visualization of the lungs in most cases, irrespective of the depth of the main target of the examination. Considering their higher radio-sensitivity , children may especially benefit from a non-ionizing technique such as LUS, above all in chronic disease or during intensive care unit stay, where the cumulative radiation dose can reach high levels [62, 63].
LUS limitations are essentially patient-dependent. Obese patients may be more difficult to examine due to the thickness of their ribcage and soft tissues. The presence of subcutaneous emphysema or large thoracic dressings alters or precludes the propagation of the ultrasound beams to the subpleural lung parenchyma.
It should be emphasized that LUS does not rule out pulmonary abnormalities that do not reach the pleura. This physical limitation is especially important when ruling out consolidations, since some consolidations, especially in the case of tumors, can be medially located and surrounded by aerated lung, which will prevent their visualization by sonography. The pulmonary interstitial syndrome from different etiologies sometimes may spare (although rarely) the subpleural space. A focal interstitial syndrome can sometimes be the “peripheral alarm” of a more medial pathological condition, for example in the case of peri-lesional interstitial edema, due to either inflammation or impaired lymphatic drainage.
While application of ultrasound for the detection of pleural effusions and masses is well established, the sonographic assessment of the lung parenchyma is relatively new. We can perform LUS for evaluating both lung parenchyma and pleural space quite easily, after a relatively brief learning curve that is significantly shorter than for other sonographic techniques, although it still requires proper training focused on the understanding of the ultrasound pulmonary semiotics and the correct clinical interpretation of the LUS patterns. LUS is very suitable for a clinically driven, point-of-care assessment that should be tailored to the clinical suspicion and the setting. In the next few years this technique is likely to become the standard of care in several acute and chronic conditions.
The authors would like to thank Alison Frank who revised the English version of the manuscript.
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