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).
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.
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 . 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 . Basic ultrasound principles in the identification of specific disorders are discussed in the next section.
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).
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.
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).
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.
This section will describe the most common disorders encountered in critical care.
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).
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) .
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 . 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 . It is important to keep in mind that lung ultrasound is more useful in excluding than confirming a pneumothorax.
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.
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 .
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.
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.
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 .
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.
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.
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).
1▪. Troianos CA, Hartman GS, Glas KE, et al. Guidelines for performing ultrasound guided vascular cannulation: recommendations of the American Society of Echocardiography and the Society of Cardiovascular Anesthesiologists. J Am Soc Echocardiogr 2011; 24:1291–1318.
One of the many internationnal guidelines published on the use of POCUS.
2▪. Rupp SM, Apfelbaum JL, Blitt C, et al. Practice guidelines for central venous access: a report by the American Society of Anesthesiologists Task Force on Central Venous Access. Anesthesiology 2012; 116:539–573.
One of the many internationnal guidelines published on the use of POCUS.
3. Thomas HA, Beeson MS, Binder LS, et al. The 2005 model of the clinical practice of emergency medicine: the 2007 update. Acad Emerg Med 2008; 15:776–779.
4. Emergency Ultrasound Guidelines. Ann Emerg Med 2009; 53:550–570.
5▪. International expert statement on training standards for critical care ultrasonography. Intensive Care Med 2011; 37:1077–1083.
One of the many international guidelines published on the use of POCUS, also stressing the importance of a structured curiculum.
6. Royal College of Physicians and Surgeons of Canada. Objectives of Training in Emergency Medicine; 2011.
7. Heller MB, Mandavia D, Tayal VS, et al. Residency training in emergency ultrasound: fulfilling the mandate. Acad Emerg Med 2002; 9:835–839.
8. Socransky S. Emergency department targeted ultrasound: 2006 update. CJEM 2006; 8:170–174.
9. Šustić A, Protić A, Cicvarić T, Župan Ž. The addition of a brief ultrasound examination to clinical assessment increases the ability to confirm placement of double-lumen endotracheal tubes. J Clin Anesth 2010; 22:246–249.
10▪▪. Ueda K, Ahmed W, Ross AF. Intraoperative pneumothorax identified with transthoracic ultrasound. Anesthesiology 2011; 115:653–655.
First study of a pneumothorax diagnosed by ultrasound in the operating room significantly changing the intraoperative course of the patient.
11▪▪. Johnson DW, Oren-Grinberg A. Perioperative point-of-care ultrasonography: the past and the future are in anesthesiologists’ hands. Anesthesiology 2011; 115:460–462.
Editorial stressing the importance of implementing POCUS in the operating room as well as in general anesthysiology practice.
12▪▪. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012; 38:577–591.
First evidence-based guidelines published on the use of POC lung ultrasound.
13. Lichtenstein D, Meziere G. A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact. Intensive Care Med 1998; 24:1331–1334.
14. Volpicelli G, Mussa A, Garofalo G, et al. Bedside lung ultrasound in the assessment of alveolar-interstitial syndrome. Am J Emerg Med 2006; 24:689–696.
15. Rantanen NW. Diseases of the thorax. Vet Clin North Am Equine Pract 1986; 2:49–66.
16. Salen PN, Melanson SW, Heller MB. The focused abdominal sonography for trauma (FAST) examination: considerations and recommendations for training physicians in the use of a new clinical tool. Acad Emerg Med 2000; 7:162–168.
17. Lichtenstein D, Meziere G, Biderman P, Gepner A. The comet-tail artifact: an ultrasound sign ruling out pneumothorax. Intensive Care Med 1999; 25:383–388.
18. Lichtenstein D, Meziere G, Biderman P, et al. The comet-tail artifact. An ultrasound sign of alveolar-interstitial syndrome. Am J Respir Crit Care Med 1997; 156:1640–1646.
19. Lichtenstein DA, Meziere GA. Relevance of Lung ultrasound in the diagnosis of acute respiratory failure: The BLUE Protocol. Chest 2008; 134:117–125.
20. Lichtenstein D, Goldstein I, Mourgeon E, et al. Comparative diagnostic performances of auscultation, chest radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004; 100:9–15.
21. Lichtenstein D, Meziere G, Biderman P, Gepner A. The ‘lung point’: an ultrasound sign specific to pneumothorax. Intensive Care Med 2000; 26:1434–1440.
22. Blaivas M, Lyon M, Duggal S. A prospective comparison of supine chest radiography and bedside ultrasound for the diagnosis of traumatic pneumothorax. Acad Emerg Med 2005; 12:844–849.
23. Blaivas M, Tsung JW. Point-of-care sonographic detection of left endobronchial main stem intubation and obstruction versus endotracheal intubation. J Ultrasound Med 2008; 27:785–789.
24. Drescher MJ, Conard FU, Schamban NE. Identification and description of esophageal intubation using ultrasound. Acad Emerg Med 2000; 7:722–725.
25. Hsieh KS, Lee CL, Lin CC, et al. Secondary confirmation of endotracheal tube position by ultrasound image. Crit Care Med 2004; 32:S374–S377.
26. Weaver B, Lyon M, Blaivas M. Confirmation of endotracheal tube placement after intubation using the ultrasound sliding lung sign. Acad Emerg Med 2006; 13:239–244.
27. Ma G, Davis DP, Schmitt J, et al. The sensitivity and specificity of transcricothyroid ultrasonography to confirm endotracheal tube placement in a cadaver model. J Emerg Med 2007; 32:405–407.
28. Milling TJ, Jones M, Khan T, et al. Transtracheal 2-d ultrasound for identification of esophageal intubation. J Emerg Med 2007; 32:409–414.
29. Werner SL, Smith CE, Goldstein JR, et al. Pilot study to evaluate the accuracy of ultrasonography in confirming endotracheal tube placement. Ann Emerg Med 2007; 49:75–80.
30. Park SC, Ryu JH, Yeom SR, et al. Confirmation of endotracheal intubation by combined ultrasonographic methods in the Emergency Department. Emerg Med Australas 2009; 21:293–297.
31. Galicinao J, Bush AJ, Godambe SA. Use of bedside ultrasonography for endotracheal tube placement in pediatric patients: a feasibility study. Pediatrics 2007; 120:1297–1303.
32. Kerrey BT, Geis GL, Quinn AM, et al. A prospective comparison of diaphragmatic ultrasound and chest radiography to determine endotracheal tube position in a pediatric emergency department. Pediatrics 2009; 123:e1039–e1044.
33. Mayo PH, Beaulieu Y, Doelken P, et al. American College of Chest Physicians/La Societe de Reanimation de Langue Francaise statement on competence in critical care ultrasonography. Chest 2009; 135:1050–1060.