INTRODUCTION
Point-of-care ultrasound (POCUS) in critical care medicine and anesthesiology is rapidly evolving and becoming the standard of care in multiple clinical situations, such as central venous access [1▪]. The American Society of Anesthesiology, the American Society of Echocardiography, and the Society of Cardiovascular Anesthesiologists have recently published specific guidelines, following the 2001 study of the Agency for Healthcare Research and Quality [1▪,2▪]. Multiple international critical care societies established guidelines concerning the use of ultrasound in their various fields of expertise as well as part of residency training [3,4,5▪,6–8]. Ultrasound is a tool widely used in the evaluation of the hypoxic patient. Indeed, multiple studies have been published in the last 20 years on the subject. Most of the literature on lung ultrasound is based on studies done in intensive care suites as well as in emergency departments, but more recently, anesthesiologists have reported their experience using lung ultrasound in the operating room [9,10▪▪]. A recent editorial article stressed the need to implement POCUS in the operating room [11▪▪]. Evidence-based recommendations have been published on POC lung ultrasound [12▪▪]. The current article will describe the basic lung ultrasound technique and the knowledge required in order to diagnose and treat the hypoxic patient. We will stress the role of lung ultrasound in the diagnosis of pneumothorax, alveolar and interstitial lung disease, and pleural effusion.
HOW TO PROCEED
All portable ultrasound machines permit us to evaluate the hypoxic patient. Recent guidelines recommended the use of an abdominal or microconvex probe, but a linear high-frequency probe can also be used [12▪▪]. In the operating room, as we will see, transesophageal echocardiography (TEE) can also be used in patients in whom the chest is not accessible such as during cardiac surgery (Fig. 1).
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FIGURE 1: Different ultrasound transducers used to perform thoracic and
lung ultrasound. The linear array (a), the phased array (note the simple
pleural effusion) (b), the convex (c) and the transesophageal echocardiography transducer (note the complex
pleural effusion) (d).(See Supplementary Digital Content 1, 2 and 3,
https://links.lww.com/COAN/A15,
https://links.lww.com/COAN/A16,
https://links.lww.com/COAN/A17.)
no caption available
Lung ultrasound can be done in a sitting or supine patient. There are generally two imaging planes that are used: the sagittal and the coronal plane (Fig. 2). As most patients in the operating rooms are in a supine position, this approach will be discussed here. A recent scanning protocol suggests a four zones division of each hemithorax in order to expedite lung ultrasound in critical situations [13,14]. Volpicelli's zones are shown in Fig. 3. Different imaging modalities are used depending on expected disorder. Most of the scanning is done in two-dimensional, but motion mode (M-Mode) as well as color Doppler can be used.
FIGURE 2: Imaging plane used in lung ultrasound scanning. A combination of sagittal (a) and coronal (b) views are used. (Image obtained from CAE Healthcare Vimedix Simulator.)
FIGURE 3: The four Volpicelli's zones. AAL, anterior axillary line; PAL, posterior axillary line.
Each thoracic zone should be scanned individually. The transducer is apposed perpendicular to the long axis of the ribs in order to obtain an image of two ribs cut in a transverse fashion (Fig. 4). The hyperechogenic linear structure between the two ribs is the pleural interface. The parietal and visceral pleura creating this interface move in a synchronous fashion with spontaneous respiration or mechanical ventilation. This movement, called ‘lung sliding’, described originally in veterinary medicine, is one of the most important findings during any ultrasound examination of the lung [15]. Lung sliding identification is the most commonly used artefact in the exclusion of pneumothorax as well as in the confirmation of endotracheal intubation (discussed later). The lung parenchyma located under the pleural interface is wherein artefacts are observed. All zones on each hemithorax must be scanned in order to obtain a complete examination. Both abdominal lateral upper quadrants can also be examined in search of pleural effusions. In the operating room, TEE use will be useful in order to detect pleural fluid, atelectasis, or pneumonia but is more limited in the detection of lung sliding [16]. Basic ultrasound principles in the identification of specific disorders are discussed in the next section.
FIGURE 4: Typical lung ultrasound image obtained with a linear transducer at 4 cm deep. The main components are identified.
BASIC ULTRASOUND PRINCIPLES
Ultrasounds are sound waves with a frequency higher than what can be perceived by the human ear. An ultrasound wave travels at approximately the same speed in all human tissue that absorbs and reflects part of it. Depending on the amount of energy absorbed as well as the time between the emission and reception of the ultrasound wave by the transducer, the software is able to generate an image depicting the underlying structures. Ultrasounds are completely reflected by air, so it is impossible in theory to see the air-filled lung parenchyma. In both normal and abnormal conditions, the thoracic cavity and the lungs may contain some physiologic or pathologic fluid. This fluid changes the relation between the ultrasound wave and the air contained in the alveolar interstitial space of the parenchyma or in the pleural space and creates particular artifacts. It is often quoted that lung ultrasound makes facts out of artefacts. After lung sliding, the most common artefacts in lung ultrasound are named A lines and B lines.
As mentioned earlier, air will reflect ultrasounds entirely as a mirror does with light. The A line artefact is the single or multiple horizontal reflections of the pleural interface. The emitted ultrasound wave is reflected multiple times by the pleural interface. This back and forth phenomenon gives a false impression to the imaging software that the pleural interface is deeper. Each A line is separated by a distance equivalent to the thickness of the subcutaneous tissue between the ultrasound probe and the pleural interface. A lines are present in a normal lung as well as in the presence of a pneumothorax (Fig. 5).
FIGURE 5: Typical lung ultrasound image obtained with a linear transducer at 6 cm deep. Note the horizontal A lines that were present in this patient. In the absence of lung sliding, this would be suggestive of a pneumothorax.
The most useful artefact, created by the reflection on air of the ultrasound wave, is known as the B line, also called comet-tail artefact or lung rocket. This artefact is created by repetitive reflections of the ultrasound wave within the lung parenchyma because of a higher concentration of physiologic or pathologic fluid [13,17]. This artefact is a vertical white line, originating from the visceral pleura, and reaching the bottom of the screen (Fig. 6). The presence of B lines will erase the A lines on their passage. Few B lines can be seen in a healthy lung typically in the dependent regions. The presence of B lines is used in the diagnosis of alveolar interstitial syndrome. The presence of B lines will automatically exclude the presence of a pneumothorax.
FIGURE 6: Typical
lung ultrasound image obtained with a linear transducer at 4 cm deep. Note the vertical B lines. These are white vertical white lines originating from the pleural interface and reaching the bottom of the screen. (See Supplementary Digital Content 4,
https://links.lww.com/COAN/A18.)
M-Mode is used in thoracic and lung ultrasound. In the presence of a normal lung, the movement of the underlying lung will create a fuzzy image under the fixed subcutaneous tissue. This pattern is often referred to as the ‘seashore’ sign. This image has two portions. The superficial part is typically composed of multiple horizontal lines that correspond to the motionless soft tissue. This image ends on the pleural line. The other portion corresponds to the motion of the normal lung. This motion will generate an artefact that originates from the pleural line and looks like sand on a beach. This double-image artefact looks like water waves in the ocean and is called the seashore or beach sign (Fig. 7).
FIGURE 7: Typical lung ultrasound image obtained with a linear transducer at 6 cm deep. A normal motion mode is shown with the seashore sign.
Using two-dimensional imaging, the ‘lung pulse’ artefact is a small to and fro movement of the visceral on the parietal pleura induced by the heartbeat that can be confused with a normal lung sliding. Although it does not constitute a normal lung sliding, it implies an intact pleural interface. It can also be identified on M-Mode imaging as an intermittent vertical artefact synchronous with the electrocardiogram. The use of color Doppler can facilitate recognition of this artefact (Fig. 8). The presence of a lung pulse artefact excludes a pneumothorax.
FIGURE 8: Typical lung ultrasound image obtained with a linear transducer at 5 and 6 cm deep. The motion mode shows regular artefact. This corresponds to lung pulse (white arrows) (a). Adding color Doppler to the motion mode image and the electrocardiogram facilitates lung pulse identification (white arrows) (b).
BASIC DISORDER
This section will describe the most common disorders encountered in critical care.
NORMAL LUNG
A normal lung is usually characterized by the presence of the following artefacts: lung sliding, A lines, less than 3 B lines per Volpicelli's sonographic zone as well as absence of pleural effusion [18,19].
ALVEOLAR INTERSTITIAL DISEASE
B lines are the major characteristic of alveolar interstitial disease. Previous studies showed that B lines separated by less than 3 mm are a sign of alveolar as opposed to interstitial lung disease [18,20]. Alveolar interstitial disease can be diffuse as in cardiogenic (Fig. 9) or noncardiogenic pulmonary edema such as acute respiratory distress syndrome (ARDS) (Fig. 10), interstitial pneumonias, and pulmonary fibrosis. They can be bilateral or limited to one part of the lung and associated with lobar pneumonia, pulmonary contusion, or atelectasis. The same constellation of artefacts will be seen for each of these disorders, but their distribution will vary depending on the spread of the disease. In the presence of ARDS as well as pneumonia, impaired lung sliding is possible. This finding can help make the difference between cardiogenic pulmonary edema in which sliding will be preserved and ARDS wherein it can be altered. In the presence of pneumonia or atelectasis, consolidated lung parenchyma can also be seen, having a similar aspect to liver parenchyma (Fig. 11).
FIGURE 9: An 83-year-old man with heart failure before cardiac surgery. Thoracic examination using a phased array transducer shows B lines on the chest wall (a). The same artefact is also present on the transesophageal echocardiographic examination at the aortic arch level (b). Corresponding chest radiograph (c). Ao, aorta.
FIGURE 10: Bilateral B lines (a,b) in a patient with acute respiratory distress syndrome. The corresponding chest radiograph (c) and computed tomography of the chest are shown (d). (See Supplementary Digital Content 5,
https://links.lww.com/COAN/A19.)
Patient with left lower lobe pneumonia. The lung parenchyma has the same aspect as liver on ultrasound, hence the word lung hepatization used in pathology. However hyperechoic elements corresponding to air bronchograms are present (a). Corresponding chest radiograph (b) and computed tomography (c). (See Supplementary Digital Content 6,
https://links.lww.com/COAN/A20.)
PNEUMOTHORAX
Pneumothorax is the disorder that made lung ultrasound gain so much popularity in the recent decade. Lung ultrasound is mostly useful in excluding the presence of pneumothorax by detecting normal lung sliding, a lung pulse, and if present, B lines. A recent case report describes the diagnosis of an intraoperative pneumothorax using lung ultrasound in two different patients. This diagnosis had a significant impact on the intraoperative course of these patients [10▪▪]. Ruling out a pneumothorax in a hypoxic mechanically ventilated patient who underwent central venous access is critical. A complete bilateral lung ultrasound in search of pneumothorax can be done in less than 3 min.
The diagnosis of pneumothorax is fairly simple. The pleural interface must be identified and examined in search of lung sliding. In the presence of a pneumothorax, air will be present between the parietal and the visceral pleura. As air completely reflects ultrasound waves, the visceral pleura will not be seen, and there will be no lung sliding. At the border of the pneumothorax, the pleural interface should be intact, and normal lung sliding should be present. This transition point between the intermittent presence and absence of a lung sliding is called the ‘lung point’. This is a pathognomonic sign of the presence of pneumothorax (Fig. 12) [21].
FIGURE 12: A 47-year-old man with a right-sided pneumothorax after liver transplantation. Thoracic ultrasound on the anterior chest (zone 1 and 2) shows A lines with no sliding lung (a). A more lateral position (zone 3 and 4) reveals normal sliding lung with B lines (b). The patient had no right superior vena cava that explains the unsuccessful attempt in inserting the right internal jugular. Note on the chest radiograph (c) the position of the pulmonary artery catheter in the left superior vena cava and through the coronary sinus. Note also the transesophageal echocardiography probe used for postoperative monitoring.
Use of M-Mode facilitates exclusion of a pneumothorax. If the seashore sign is present, there is no pneumothorax in the part of the lung scanned [21]. If there is a pneumothorax, the absence of lung sliding will create a series of black and white horizontal lines, called the ‘stratospheric or barcode’ sign. The lung point can also be identified on M-Mode as a transition between a seashore sign and a barcode sign (Fig. 13). The lung point, seen on M-Mode or conventional two dimensional, is 100% specific for pneumothorax [21]. It is important to keep in mind that lung ultrasound is more useful in excluding than confirming a pneumothorax.
FIGURE 13: Same patient as in Figure 12. The postoperative right-sided pneumothorax is seen on the chest radiograph (a). The barcode (or stratospheric) aspect of the motion mode followed by the normal seashore sign. This transition is called a lung point and is diagnostic of the pneumothorax (b).
Caution must be taken if a lung point is identified in the lower parts of the lungs. The excursion of the diaphragm, for instance, above the liver can give a false impression of lung point. This phenomenon can be called the ‘abdominal point’ (Fig. 14). Absent lung sliding can also be encountered in an unventilated lung, severe ARDS, or lung atelectasis. Caution must also be taken if a lung pulse is identified close to the sternum as pulsation of a mammary artery could lead to false exclusion of pneumothorax. Color Doppler and pulsed-wave Doppler interrogation can confirm the arterial origin of this structure.
FIGURE 14: Saggital view at the level of the interface between the lung and the liver. This interface corresponds to the abdominal point (a). Corresponding motion mode view. Note the transition points (white arrows). During inspiration the motion mode artefact are seen. They correspond to the normal lung (between the arrows). During expiration, the motion mode aspect of the liver is seen (lateral portion of the image outside the arrow). This can be easily seen by also using two-dimensional echocardiography. (See Supplementary Digital Content 7,
https://links.lww.com/COAN/A21.)
If A lines are seen with no lung sliding, no B lines, no lung pulse, and no lung point is identified, a pneumothorax is probable. However, the identification of a lung point is essential to confirm the presence of a pneumothorax. In the absence of the lung point, alternative methods of diagnosis are suggested in a nonlife-threatening situation, remembering that supine chest radiograph is not very sensitive to detect a pneumothorax.
A rapid scanning protocol concentrating on the second intercostal space on the midclavicular line, the fourth intercostal space on anterior axillary line, the sixth intercostal space on the midaxillary line, and the eighth intercostal space on the posterior axillary line showed a sensitivity of 98.1% and specificity of 99.2% in the diagnosis of pneumothorax with lung ultrasound [22].
PLEURAL EFFUSIONS
Thoracic ultrasound can rapidly identify simple or complex pleural effusions. In a supine patient, using a microconvex, phased array or convex transducer, both abdominal upper quadrants on the middle or the posterior axillary line should be scanned in order to view the interface between the diaphragm and the lung, just above the liver and the spleen [12▪▪]. The air contained in a normal lung parenchyma will reflect the ultrasound waves bouncing off the liver or the spleen and create an image identical to these structures. In the presence of a pleural effusion, this normal mirror image is lost and liquid is seen. Through this effusion, parts of the lung can be visualized. A simple effusion will be homogeneous, but a complex effusion, such as a hemothorax or an empyema, will be heterogeneous (Fig. 15). Caution must be taken not to mistake free peritoneal fluid, located under the diaphragm, as a pleural effusion.
FIGURE 15: A 67-year-old woman presented with sudden hypotension and shortness of breath. She was started on low-molecular weight heparin, 3 days ago for lower extremity deep venous thrombophlebitis. Upon examination, breath sound was reduced on the left side. Bedside cardiac function was normal with signs of hypovolemia. Thoracic ultrasound revealed an isoechoic mobile mass corresponding to an hematoma (a) that was confirmed on chest radiograph (b) and computed tomography (c). A chest tube was inserted.
OTHER USES OF THORACIC AND LUNG ULTRASOUND
POC thoracic and lung ultrasound is a very useful tool in critical care medicine. It can be used to confirm endotracheal intubation, the correct placement of a double-lumen endotracheal tube, or to identify a mainstem intubation [9,23]. Methods used to confirm endotracheal intubation by ultrasound include lung sliding identification, visualization of diaphragm movement, and direct endotracheal tube visualization in the trachea or oesophagus [24–30]. Ultrasound can also be used to confirm endotracheal intubation in pediatric patients [31,32].
Diaphragmatic movement identification in a breathing patient also permits us to exclude a complete diaphragmatic paralysis after procedures such as interscalene block, high abdominal surgery, or internal mammary artery manipulation in a coronary bypass surgery.
LIMITATIONS
As air creates significant impedance to ultrasound penetration, thoracic and lung ultrasound is impossible in patients with subcutaneous emphysema. Deeper lung disorder is not adequately investigated because only superficial portions of the lung are accessible to ultrasound. In addition, in severely obese patients or women with large breasts, ultrasound examination might be limited. Pulmonary embolism is also not easily identified by lung ultrasound. In massive pulmonary embolism, the lung ultrasound examination will be typically normal. Complementary POCUS of the heart and lower extremities will be necessary. Finally POCUS remains operator dependent, and a structured formation is needed such as the one proposed by the American College of Chest Physician [33].
APPROACH OF THE HYPOXIC PATIENT
Depicted in Fig. 16 is a rapid thoracic and lung ultrasound protocol for the hypoxic patient. This protocol contains the basic lung and thoracic ultrasound elements discussed in the previous paragraphs.
FIGURE 16: Thoracic and lung ultrasound protocol to investigate the hypoxic patient.
CONCLUSION
Thoracic and lung ultrasound are very useful tools in the evaluation of the hypoxic patient. This situation can occur in the operating room, recovery room, the ICU and the emergency ward. Its ease of access, mobility, rapidity, repeatability, and lack of radiation gives it an advantage over chest radiograph and computed tomography. Bedside ultrasound is already used for central venous accesses and nerve blockade. Expansion of its use in the thoracic region and the abdomen is a natural evolution. Combined with pulse oximetry, end-tidal carbon dioxide monitoring, mechanical ventilation monitors and bronchoscopy, thoracic and lung ultrasound will allow investigating almost every cause of hypoxemia. Training guidelines have already been published. Structured curriculum in anesthesiology, critical care, and emergency medicine will enable a well tolerated and precise use of thoracic and lung ultrasound.
Acknowledgements
We would like to thank Mr Denis Babin for his graphical help. Dr A.D. received consulting fees/honoraria from Coviden Speaker Bureau.
Conflicts of interest
There are no conflicts 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
Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 100).
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