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Evaluation of Pulmonary Emergencies Using Point-Of-Care Ultrasound in the Pediatric Emergency Department: A Review
Abstract: Point-of-care ultrasound has a wide array of applications in the emergency care of children. Over the past 3 decades, lung ultrasound has evolved and become an asset in evaluating both emergent and critically ill patients. Ultrasound of the lung was once thought to be of little utility because normal lung is aerated and ultrasound cannot directly visualize air. Thus, it was unclear how ultrasound would be beneficial. It is now evident that ultrasound of the chest is extremely useful in evaluating not only normal lung but also pathologic conditions. This article reviews the clinical utility of point-ofcare transthoracic lung ultrasound in the diagnosis of pneumothorax, lung consolidations, interstitial syndromes, and pleural effusions.
Keywords: point-of-care ultrasound; bedside ultrasound; pediatric emergency ultrasound; lung ultrasound; pneumothorax; pneumonia; pleural effusion; alveolar-interstitial syndrome
*Division of Emergency and Transport Medicine, Children's Hospital Los Angeles, Keck School of Medicine/University of Southern California, Los Angeles, CA 90027; †Division of Emergency Medicine, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, DC. Reprint requests and correspondence: Joshua Sherman, MD, Division of Emergency and Transport Medicine, Children's Hospital Los Angeles, Keck School of Medicine/University of Southern California, Los Angeles, CA 90027. [email protected] (J.M. Sherman), [email protected] (A.M. Abo) 1522-8401 © 2015 Elsevier Inc. All rights reserved.
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Evaluation of Pulmonary Emergencies Using Point-OfCare Ultrasound in the Pediatric Emergency Department: A Review Joshua M. Sherman, MD*, Alyssa M. Abo, MD†
P
oint-of-care ultrasound (POCUS) has a wide array of applications in the pediatric emergency department (ED). Over the past 3 decades, lung ultrasound (LUS) has evolved and become an asset in evaluating both emergent and critically ill patients. Ultrasound (US) of the lung was once thought to be of little utility because normal lung is aerated and US cannot directly visualize air. Thus, it was unclear how US would be beneficial. It is now apparent that US of the chest is extremely useful in evaluating not only normal lung but also pathologic conditions such as pneumothorax, consolidations, interstitial syndromes, and pleural effusions. The key to understanding how LUS works is rooted in US physics and artifacts, and
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specifically, how US waves behave when they encounter an aerated vs pathologic lung.
BACKGROUND Point-of-care transthoracic lung ultrasound (TTLUS) was first developed and proven beneficial in adults and more recently adapted to pediatrics. In emergency and critical care settings, the role of TTLUS has traditionally been used to evaluate pleural effusions and to guide thoracocentesis. 1 However, beginning in the 1980s, there were reports that US could be used to identify patients with pneumothorax 2 as well as pneumonia. 3 Subsequently, in the 1990s, Lichtenstein et al 4 -7 began reporting their findings of bedside LUS in the intensive care unit. These initial studies identified many of the artifacts that are crucial to LUS and laid the foundation of point-of-care LUS. The term artifact is used to explain a by-product of US that is displayed on the screen when sound waves encounter a certain medium, but in reality is not there. In the early 2000s, emergency physicians began publishing data on point-of-care LUS in adults in the ED. Many of the initial studies were related to pneumothorax, and by 2004, Kirkpatrick et al 8 described the evaluation of pneumothorax as part of the trauma evaluation. These data, along with other case reports and studies, 9 -11 ultimately led to incorporating LUS into the focused assessment with sonography in trauma (FAST) examination, which is now termed the extended FAST or EFAST. 12 At the same time, research was underway to understand how LUS could play a part in the diagnosis and management of other disease processes. In 2005, Mathis et al 13 demonstrated its ability to diagnose pulmonary embolism, whereas Reissig and Kroegel 14 showed its utility in diagnosing and following pneumonia in 2007. Transthoracic lung ultrasound has been proven to be useful in adult disease states such as pulmonary embolism, 15 -20 acute respiratory distress syndrome, 21 and acute respiratory failure. 22 In 2012, international evidence-based recommendations for point-of-care LUS, including pediatric data, were published, reinforcing the use of POCUS for lung evaluation in children. 23 Over the past 15 years, research has been published regarding LUS in pediatrics; however, available data mainly address pneumonia and other infectious processes. There is little published research regarding LUS and the diagnosis of pneumothorax in the pediatric population. Therefore, pediatric emergency specialists have incorporated point-of-care
TTLUS in the pediatric population based largely on the literature from the emergency care of adults. This article reviews the clinical utility of pointof-care TTLUS, in pediatric emergency and critical care medicine, in the diagnosis of pneumothorax, lung consolidations, interstitial syndromes, and pleural effusions. The evidence and sonographic findings specific to each of these disease processes will be reviewed, and the future of point-of-care TTLUS in pediatrics will be discussed.
LUNG ULTRASOUND: PRINCIPLES AND TECHNIQUE The advantage of POCUS is multifold. Bedside US can be performed concurrently with the physical examination, expanding the data available to the clinician in real-time, and is rapid and repeatable. Another major advantage is that US does not produce any ionizing radiation. In an era where efforts are made to comply with the ALARA (as low as reasonably achievable) principle regarding radiation exposure, US reduces the radiation exposure for pediatric patients. There are a few disadvantages of which the sonographer should be cognizant. First and foremost, US is operator dependent. Therefore, clinicians must be properly trained in POCUS of the lung and deemed competent before making medical decisions based on the results. In addition, US is unable to visualize pathology below aerated lung; the disease process must extend to the pleura to be identified. Thus, any pathology lying below aerated lung will not be visualized. The key to understanding LUS is based on physics and artifacts. In simple terms, US cannot travel through air without getting scattered and reflected; therefore, when the lung is aerated the sonographer can only visualize the ribs and the pleural surface between the ribs (Figure 1). In older children, the ribs will produce anechoic “black” shadows because the US cannot pass through bone (Figure 1). However, in younger children, the bones are cartilaginous and therefore do not produce the same shadows (Figure 2). Below the pleura is aerated lung, which the sonographer cannot directly see. What can be seen are reflections of the pleural line, which are termed A lines. These A lines are horizontal lines that are a result of sound reverberating or bouncing between the pleura and the transducer; hence, the A lines are equidistant from one another (Figure 1). The pleura between the 2 ribs will give a shimmering effect because of the to-and-fro movement of the 2 layers
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Figure 1. Normal lung, showing the pleura, A lines, and ribs (*).
of the pleura rubbing against one another. This is termed lung sliding and cannot be appreciated in a still image (Video 1). In the case of a pneumothorax, there is no lung sliding. In addition to lung sliding, there are comet tail artifacts that arise from the interface of pleural sliding with air. Small comet tail artifacts called “Z lines” are normal, they fade, and they do not disrupt the A line pattern (Figure 3). To the contrary, “B lines,” which are also a type of comet tail artifact, are abnormal when more than a few are present. They extend from the pleura line to the edge of the screen and do disrupt the A lines (Figure 3). This disruption occurs because of fluid in the lung that allows for the transmission of sound. In addition, B lines move with lung sliding, and they do not fade. Pathology of the lung is evident when the balance of air and fluid within in the lungs changes or when there is an accumulation of air or fluid between the
Figure 2. Lung of a neonate, pleura is visible below the cartilaginous ribs (*).
Figure 3. Comet tail artifacts: Z lines on left compared to a B line on right.
pleural layers as in a pneumothorax or pleural effusion, respectively. As for consolidations and interstitial syndromes, the balance between fluid and air determines what the sonographer visualizes. In interstitial syndromes, there is more air than fluid in the lung, whereas in consolidations, there is more fluid than air. There are varying approaches to interrogating the lungs with US. Lung ultrasound techniques vary. First and foremost, the sonographer must choose an appropriate probe. High-frequency linear probes may be the probe of choice for evaluating the pleura, as their high resolution is ideal for shallow structures; the caveat being that these probes cannot evaluate structures deep in the chest. Highfrequency linear probes are also ideal for evaluating for pneumothorax. If the clinician is concerned about fluid (including interstitial syndromes, pleural effusions, or consolidations), then a phased array or
Figure 4. Base of the lung where the lung meets the diaphragm (= =).
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Figure 5. Right upper quadrant view, mirror image of the liver.
curvilinear probe would be more appropriate. These probes have lower frequency and allow for the evaluation of deeper structures. Once the probe is chosen, the next step is where to place the probe. There are varying approaches on how to evaluate the lung fields. Despite the existence of an international recommendation, there is not one standard accepted way to interrogate the lungs with US. 23 It is generally accepted that if the clinician is concerned for a pneumothorax, the probe should be placed anteriorly on the supine patient. If the concern is for fluid or another gravity-dependent process, then the clinician should interrogate the axillary and posterior lines at the base of the lung where the lung meets the diaphragm (Figure 4). A comprehensive approach, dividing the
chest in 28 zones, has been described; 24 however, division of the chest into 4 to 6 zones on each side is a more reasonable approach in the ED setting. 25 The 6 zones would include a superior and inferior view in the anterior, axillary, and posterior portion of each side of chest (12 views in total). It is also important that clinicians are aware that the lung is visible when evaluating other structures, including the inferior vena cava and the heart in the parasternal view, as well as the upper quadrant views of the FAST examination. These unconventional views can certainly identify pathology that the clinician did not expect. For example, when evaluating the right and left upper quadrants in a trauma evaluation, the area above the diaphragm is normally aerated lung, which provides a mirror image of the solid organ (spleen or liver) (Figure 5) in normal circumstances. In the case of a pleural effusion or consolidation in the chest, the lung is no longer aerated, and the sound is transmitted through the diaphragm and the spine is visualized in the chest. This is termed the spine sign (Figure 6).
APPLICATIONS Pneumothorax One of the most important applications of point-of-care TTLUS in the ED is the evaluation for pneumothorax. This lifesaving application is well studied in adult medicine and takes the provider a few minutes to perform. Answering the question, “does the patient have a pneumothorax?” can drastically change the management of the trauma patient.
Evidence
Figure 6. Spine sign: pathology in the lung allows the transmission of sound; hence, the spine if visible above the level of the diaphragm.
In 2005, Lichtenstein et al 7 published a landmark article on the use of TTLUS for evaluation of pneumothoraces. In a retrospective study spanning 10 years, the authors studied patients who received chest computed tomography (CT), chest radiograph (CXR), and US. They evaluated 43 hemithoraces with radiooccult pneumothoraces against 310 hemithoraces with no pneumothorax. Using US, they evaluated the lung for the following findings: absence of lung sliding, absence of lung sliding with A line sign, and evaluation of a lung point (the junction of normal lung sliding and absent lung sliding). Each examination only took 2 minutes. When the examination revealed absence of lung sliding, LUS had a sensitivity of 100%, specificity of 78%, negative predictive value (NPV) of 100%, and positive predictive value (PPV) of 40%. When combining the absence of lung sliding with the A
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Figure 7. M-mode image—normal lung.
line sign, the modality had sensitivity of 95%, specificity of 94%, NPV of 99%, and PPV of 71%. However, if a lung point was identified, the sensitivity of this study became 79%, and specificity rose to 100%, with NPV of 97% and PPV of 100%. The authors therefore concluded the following: (1) lung sliding rules out pneumothorax; (2) lung point rules
Figure 8. M-mode image—pneumothorax.
in pneumothorax; and (3) LUS for evaluation of pneumothorax has high feasibility, high sensitivity, and rapidity, with a simple technique and a short learning curve. In 2006, Zhang et al 11 evaluated trauma patients in the ED using US to detect pneumothoraces. The study showed that US was more sensitive and more
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Figure 9. Lung pulse on M-mode.
accurate than CXR in detecting pneumothorax. The authors showed that the time needed for diagnosis of pneumothorax was significantly shorter with US compared to CXR (2.3 ± 2.9 vs 19.9 ± 10.3 minutes; P b .001). The diagnostic sensitivity for detecting pneumothorax with US vs radiography was also found to be clinically significant; 86.2% vs 27.6% (P b .001). Ultrasound was highly consistent with CT in determining the size of pneumothorax (κ = 0.669; P b .001). According to the International Consortium for POCUS, 23 LUS should be used in clinical settings when the differential diagnosis includes pneumothorax. They also report strong evidence (level A) to support the statement that LUS more accurately rules out the diagnosis of pneumothorax than supine CXR. A 2014 case series demonstrated the utility of US in guiding needle placement in patients with spontaneous pneumothorax. 26 Future pediatric studies are needed to further evaluate this US-guided procedure.
Sonographic Findings The normal lung is characterized by lung sliding (Video 1). This sliding is a to-and-fro movement visible at the pleural line and is caused by inspiratory excursion of the lung toward the abdomen. If the clinician is unsure whether the lung is sliding, both color Doppler and motion mode can be of assistance. In normal lung, lung sliding will
produce flashes of color along the pleura line (Video 2) that will not be present in patients with pneumothorax. Normal lung also exhibits artifacts known as A lines and comet tail artifacts. In pneumothorax, while A lines persist, lung sliding and comet tail artifacts are absent as the pleural layers are now separated by air. When using motion mode (“M-mode”), normal lung sliding produces an image known as the seashore sign, which is a distinction of 2 patterns: (1) the wave-like pattern above the pleural line and (2) the sand-like pattern below the pleural line (Figure 7). In M-mode, for patients with a pneumothorax, the image will look like a barcode (“barcode sign”) or like the stratosphere (“stratosphere sign”) (Figure 8). The lung point is the transition zone from normal lung to lung affected by a pneumothorax; seashore sign and the barcode are next to each other where normal lung sliding ends and lack of movement begins. It is crucial that the M-mode caliper be placed in the middle of the pleural space. When evaluating a patient for pneumothorax, the sonographer must be familiar with both the false positives and false negatives. False-negative studies are usually those where the examination is incomplete or when there are small apical pneumothoraces that are not detected. False positives, on the other hand, are often cases where the patient has pleural adhesions or a main stem intubation. In the case of a main stem intubation, the lung will not be sliding, but
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Figure 11. Air bronchograms within the lung, a tree-like pattern.
Figure 10. A, Consolidation: Shred sign. B, Consolidations: Hepatization of the lung.
on M-mode, the sonographer may appreciate a lung pulse. The pattern is alternating between seashore and bar code and occurs because the collapsed lung is vibrating in a pulse-like fashion because of the lung's proximity to the beating heart (Figure 9).
which confirmed the presence of pneumonia. In the 3 remaining patients, the clinical course was consistent with pneumonia. Sonographic findings of pneumonia included echogenic areas with illdefined borders and the absence of lung sliding and A lines. Comet tail artifacts were sometimes seen within the consolidation. The investigators also showed that TTLUS is helpful in differentiating among types of consolidations, such as pneumonia and atelectasis, by identifying dynamic air bronchograms within the consolidation. The main limitation of this study was the authors' inability to report on the sensitivity and specificity of TTLUS because chest CT, which one might consider as an imaging criterion standard for pneumonia, was not performed on every patient for obvious ethical reasons. The other limitations were that: (1) no lateral CXR was obtained, only a single anterior-posterior view
Consolidations Evidence In 2008, Copetti and Cattarossi 27 published a landmark article that compared the diagnostic accuracy of point-of-care TTLUS and CXR in children with suspected pneumonia. Seventy-nine children from 6 months to 16 years of age with clinical symptoms of pneumonia such as cough, tachypnea, crackles, and decreased breath sounds were studied. Ultrasound was positive in 60 patients, whereas CXR was positive in 53. Of the 7 patients with a negative CXR and positive US, 4 underwent chest CTs (performed for recurrent pneumonia),
Figure 12. Multiple B lines.
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was taken, and (2) sonography was only performed by one clinician who was an expert in sonography. In 2012, Shah et al 28 increased the sample size and published a study aimed at determining the accuracy of point-of-care TTLUS for the diagnosis of pneumonia in children and young adults. This was a prospective observational cohort study involving 200 patients from 2 different EDs. Ultrasound examinations were performed by 15 different emergency medicine physicians with varying levels of expertise after a 1-hour LUS training session. Children aged 0 to 21 years undergoing a CXR for suspicion of pneumonia were included in the study. In this study, they used CXR as the criterion standard. By visualizing consolidation with sonographic air bronchograms, TTLUS had a sensitivity of 86% and specificity of 89%, with a positive likelihood ratio of 7.8 and a negative likelihood ratio of 0.2. Interestingly, for a subgroup of 187 patients who had a consolidation of greater than 1 cm, the specificity increased to 97% and the positive likelihood ratio to 28, while the negative likelihood ratio decreased to 0.1. The authors concluded that clinicians are able to diagnose pneumonia in children and young adults using POCUS with high specificity. The 2012 International Guidelines published gave very strong recommendations regarding TTLUS for the diagnosis of pneumonia. 23 The authors concluded that LUS is as accurate as CXR in the diagnosis of pneumonia in pediatric patients. Furthermore, LUS for the detection of lung consolidation should be used because it can differentiate consolidations due to pulmonary embolism, pneumonia, or atelectasis, based on visualization of sonographic air bronchograms. It is noted that LUS should be considered an accurate tool in detecting consolidation when compared to CXR. In addition, in mechanically ventilated patients, LUS is more accurate than portable CXR in detection of consolidation. It is important to note that according to this source, LUS does not rule out consolidations that do not reach the pleura. More recently, in 2014, Esposito et al 29 published a prospective observational study regarding the performance of TTLUS in diagnosing community-acquired pneumonia. They included otherwise healthy children aged 1 month to 14 years who were admitted to the hospital with fever and clinical signs and symptoms of community-acquired pneumonia, such as cough, tachypnea, respiratory distress, grunting, wheezing, or rales. Anterior-posterior as well as lateral CXR images were obtained and read by a radiologist. Transthoracic lung ultrasound was performed by pediatric residents who had partici-
pated in a 1-day LUS course. They reported that when compared to CXR, TTLUS had a sensitivity of 97.9% and specificity of 94.5% with a PPV of 94% and an NPV of 98.1%. In addition, TTLUS was found to detect higher numbers of pleural effusions. In 2015, Pereda et al 30 published a meta-analysis of studies involving LUS for the diagnosis of pneumonia in children. They reported LUS as having a sensitivity of 96% and specificity of 93%, with a positive likelihood ratio of 15.3 and a negative likelihood ratio of 0.06. The authors concluded that current evidence does support LUS as an imaging alternative for the diagnosis of childhood pneumonia and advocate for the training of pediatricians in LUS.
Sonographic Findings There are a number of sonographic findings described with consolidations, including the shred sign and the tissue sign. Consolidations of the lung are filled with more fluid than air and therefore are well delineated. These areas are echogenic and are often surrounded by pleural effusions. The shred sign is when the edge of the pleura looks irregular and shredded (Figure 10A); the tissue sign, also referred to as hepatization of the lung, is when the lung begins to look like the liver (Figure 10B). In the latter image, not only does the lung look like liver, but it is surrounded by a pleural effusion, and the spine is visible above the level of the diaphragm. Vertical artifacts can sometimes be seen within the consolidation. These may be comet tail artifacts but are different than B lines as they do not originate at the pleural line but rather from within the consolidation. In addition, air bronchograms may occasionally appear as branching echogenic structures within the consolidation (Figure 11). Dynamic air bronchograms, in which the movement of air with breathing is visible within the consolidation, rule out atelectasis. 31
Alveolar-Interstitial Syndromes Several interstitial disease syndromes can be identified with POCUS. In adult emergency medicine, the most commonly identified interstitial syndrome is pulmonary edema, often seen in patients with congestive heart failure or fluid overload. Other interstitial syndromes include pulmonary contusions, pneumonia, and pneumonitis as well as bronchiolitis, which is more common in pediatrics. The hallmark finding of interstitial syndromes is the B line (Figure 3). In patients with extensive parenchymal disease, US can identify pleural and subpleural abnormalities as well.
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Figure 13. Pleural effusion.
Based on the international evidence-based recommendations, there is strong evidence to suggest that B lines are the sonographic sign of interstitial syndromes. 23 Level A recommendations state that the technique should involve scanning at least 8 regions, with 3 or more B lines in a longitudinal plane between 2 ribs indicating a positive region for interstitial disease. There is strong evidence to suggest that LUS is superior to CXR for diagnosing or excluding a significant interstitial syndrome.
Evidence Bronchiolitis. Caiulo et al 32 published a 2011 study comparing TTLUS with CXR in children aged 1 to 16 months with clinical signs and symptoms of bronchiolitis, based on the American Academy of
Figure 14. Lung edge visible within pleural effusion; positive spine sign.
Pediatrics definition. They used the Downes' Score to categorize the patients into mild, moderate, or severe bronchiolitis. They found that LUS was positive for bronchiolitis in 47 of 52 patients, whereas CXR was positive in 38 of 52 patients and concluded that LUS is a simple and reliable tool for diagnosis of bronchiolitis. The article also describes sonographic findings suggestive of bronchiolitis. However, there were many limitations to this study. As bronchiolitis is a clinical diagnosis, there is no true criterion standard. The American Academy of Pediatrics recommends against the use of routine chest radiography in children with suspected diagnosis of bronchiolitis. 33 Therefore, a “normal” CXR does not exclude the diagnosis of bronchiolitis. Further studies are needed to assess the utility of TTLUS in the diagnosis of bronchiolitis. Pulmonary Contusions. Pulmonary contusions are a possible result of blunt trauma to the chest in both pediatric and adult patients. In 2006, Soldati et al 34 investigated the utility of POCUS in diagnosing pulmonary contusions. Patients were evaluated with LUS initially, followed by CXR and CT scan. Contusions were defined as: 1. Alveolointerstitial syndrome, defined as the presence of multiple B lines arising from the pleural line, in a patient with no clinical suspicion of cardiogenic pulmonary edema. 2. Peripheral parenchymal lesion, defined as the observation of C lines, confluent consolidations (“hepatization”), or parenchymal disruption with localized pleural effusion. Patients were excluded if they had a pneumothorax. The study showed that when alveolointerstitial syndrome was used as the diagnostic criterion for pulmonary contusion, TTLUS sensitivity was 94.6%; specificity, 96.1%; PPV and NPV, 94.6% and 96.1%, respectively; and accuracy was 95.4%. When peripheral parenchymal lesion was used as the criterion, sensitivity and NPV fell to 18.9% and 63%, respectively; however, the specificity and PPV both increased to 100%. A 2009 case report described the use of POCUS in detecting a pulmonary contusion in a pediatric patient after blunt trauma. 35 The contusion was confirmed on chest CT. Future studies are needed in pediatrics regarding POCUS in trauma for both pneumothorax and pulmonary contusions.
Sonographic Findings As discussed previously, normally, the lung is filled with air and does not allow for visualization of normal lung parenchyma. As mentioned, in normal
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Figure 15. M-mode image of a pleural effusion shows a sinusoidal pattern.
lung, A lines are horizontal artifacts that are equidistant from each other, whereas B lines are vertical comet tail artifacts arising from the pleural line, reach the edge of the screen, erasing A lines, and move with normal lung sliding. Multiple B lines are the hallmark of interstitial disease and can be seen in pulmonary edema and pulmonary contusions as well as bronchiolitis. According to Caiulo et al, 32 findings consistent with bronchiolitis include presence of subpleural lung consolidations, defined as subpleural areas with a tissue-like appearance or poor echo structure with blurred margins; presence of compact B lines, defined as areas of white lung; pleural line abnormalities, defined as irregular appearance of pleural line; and the presence of focal areas with numerous B lines (Figure 12).
Pleural Effusion Evidence Lung ultrasound can be used for detecting pleural effusions. Kocijancic et al 36 demonstrated that LUS is more sensitive than lateral decubitus CXR in detection of small pleural effusions. Calder and Owens 37 established that LUS performed better than CT or magnetic resonance imaging in showing septated effusions and/empyemas.
The International Consortium for Point-of-Care Ultrasound reported with strong evidence-based recommendations that: 23 1. A pleural effusion with internal echoes suggest exudate or hemorrhage. 2. For detection of pleural effusion, LUS is more accurate than supine CXR and is as accurate as CT. 3. When a CXR identifies both opacities and effusion, an LUS should be obtained because it is more accurate than CXR in distinguishing between opacities and effusion.
Sonographic Findings In normal lung, the visceral and parietal pleura are in contact with one another; however, when a pleural effusion is present, fluid (usually anechoic) separates the pleural layers (Figure 13). Pleural effusions allow for the visualization of the spine above the diaphragm (Figure 14). On M-mode, if the caliper is placed at the edge of the lung that is surrounded by fluid, this will result in the “sinusoid sign” representing respiratory movement of the lung within the effusion (Figure 15).
FUTURE CONSIDERATIONS Point-of-care LUS has an important role in pediatric emergency medicine. Specific pediatric
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LUS research is crucial to advance the field. Protocols and algorithms would be extremely useful for clinicians and could ensure consistency among providers on how to integrate POCUS into medical decision making. Multicenter bedside US studies would greatly benefit the pediatric emergency medicine community.
SUMMARY It is evident that point-of-care LUS is in an asset in pediatric emergency medicine. Visualizing the lung in real time can aid the clinician in diagnosing pathology as well as assisting with procedures. Point-of-care ultrasound has been shown to decrease complications associated with thoracocentesis. 38 Furthermore, POCUS has been shown to reduce the number of radiographs and CT scans in critically ill adults. 39 If POCUS becomes widely accepted in pediatric emergency medicine, it can reduce the amount radiation to which children are exposed. In the meantime, clinicians with a background in POCUS are encouraged to continue exploring this interesting field of medicine.
ACKNOWLEDGMENTS Conflict of interest: None. Supplementary data (eg. videos) to this article can be found online at http://dx.doi.org/10.1016/j.cpem.2015.11.006.
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9. 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;12:844–9. 10. Chung MJ, Goo JM, Im JG, et al. Value of high-resolution ultrasound in detecting a pneumothorax. Eur Radiol 2005; 15:930–5. 11. Zhang M, Liu ZH, Yang JX, et al. Rapid detection of pneumothorax by ultrasonography in patients with multiple trauma. Crit Care 2006;10:R112. 12. Kirkpatrick AW, Nicolaou S. The sonographic detection of pneumothoraces. In: Kharmy-Jones R, Nathens A, Stern E, editors. Textbook of thoracic trauma and critical care. Boston, MA: Kluwer Academic Publishers; 2002. p. 227–34. 13. Mathis G, Blank W, Reissig A, et al. Thoracic ultrasound for diagnosing pulmonary embolism: a prospective multicenter study of 352 patients. Chest 2005;128:1531–8. 14. Reissig A, Kroegel C. Sonographic diagnosis and follow-up of pneumonia: a prospective study. Respiration 2007;74: 537–47. 15. Reissig A, Kroegel C. Diagnosis of pulmonary embolism and pneumonia using transthoracic sonography. In: Bollinger CT, Herth FJF, Mayo PH, et al, editors. Textbook of clinical chest ultrasound: from the ICU to the bronchoscopy suite. Bazel, Switzerland: Krager; 2009. p. 43–50. 16. Reissig A, Heyne JP, Kroegel C. Ancillary lung parenchymal findings at spiral CT scanning in pulmonary embolism. Relationship to chest sonography. Eur J Radiol 2004;49: 250–7. 17. Mathis G, Bitschnau R, Gehmacher O, et al. Chest ultrasound in the diagnosis of pulmonary embolism in comparison to helical CT. Ultraschall Med 1999;20:54–9. 18. Niemann T, Egelhof T, Bongartz G. Transthoracic sonography for the detection of pulmonary embolism—a metaanalysis. Ultraschall Med 2009;30:150–6. 19. Pfeil A, Reissig A, Heyne JP, et al. Transthoracic sonography in comparison to multislice computed tomography in detection of peripheral pulmonary embolism. Lung 2010; 188:43–50. 20. Torbicki A, Perrier A, Konstantinides S. Guidelines of the diagnosis and management of acute pulmonary embolism of the European Society of Cardiology (ESC). Eur Heart J 2008; 29:2276–315. 21. Copetti R, Soldati G, Copetti P. Chest sonography: a useful tool to differentiate acute cardiogenic pulmonary edema from acute respiratory distress syndrome. Cardiovasc Ultrasound 2008;6:16–25. 22. Lichtenstein DA, Meziere GA. Relevance of lung ultrasound in the diagnosis of acute respiratory failure: the BLUE protocol. Chest 2008;134:117–25. 23. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012;38:577–91. 24. Jambrik Z, Monti S, Coppola V, et al. Usefulness of ultrasound lung comets as a nonradiologic sign of extravascular lung water. Am J Cardiol 2004;93:1265–70. 25. Volpicelli G, Mussa A, Garofalo G, et al. Bedside lung ultrasound in the assessment of alveolar interstitial syndrome. Am J Emerg Med 2006;24:689–96. 26. Ng C, Tsung JW. Point-of-care ultrasound for assisting in needle aspiration of spontaneous pneumothorax in the pediatric ED: a case series. Am J Emerg Med 2014;32: 488.e3–8.
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27. Copetti R, Cattarossi L. Ultrasound diagnosis of pneumonia in children. Radiol Med 2008;113:190–8. 28. Shah V, Tunik M, Tsung J. Prospective evaluation of point-ofcare ultrasonography for the diagnosis of pneumonia in children and young adults. JAMA Pediatr 2013;167:119–25. 29. Esposito S, Papa S, Borzani I, et al. Performance of lung ultrasonography in children with community acquired pneumonia. Ital J Pediatr 2014;40:37. 30. Pereda MA, Chavez MA, Hooper-Miele CC, et al. Lung ultrasound for the diagnosis of pneumonia in children: a meta-analysis. Pediatrics 2015;135:714–22. 31. Lichtenstein D, Mezière G, Seitz J. The dynamic air bronchogram. A lung ultrasound sign of alveolar consolidation ruling out atelectasis. Chest 2009;135:1421–5. 32. Caiulo VA, Gargani L, Caiulo S, et al. Lung ultrasound in bronchiolitis: comparison with chest X-ray. Eur J Pediatr 2011;170:1427–33. 33. American Academy of Pediatrics Subcommittee on the Diagnosis and Management of Bronchiolitis. Diagnosis
34. 35. 36. 37. 38. 39.
and management of bronchiolitis. Pediatrics 2006;118: 1774–93. Soldati G, Testa A, Silva FR, et al. Chest ultrasonography in lung contusion. Chest 2006;130:533–8. Stone MB, Secko MA. Bedside ultrasound diagnosis of pulmonary contusion. Pediatr Emerg Care 2009;25:854–5. Kocijancic I, Vidmar K, Ivanovi-Herceg Z. Chest sonography versus lateral decubitus radiography in the diagnosis of small pleural effusions. J Clin Ultrasound 2003;31:69–74. Calder A, Owens CM. Imaging of parapneumonic pleural effusions and empyema in children. Pediatr Radiol 2009;39: 527–37. Mercaldi CJ, Lanes SF. Ultrasound guidance decreases complications and improves the cost of care among patients undergoing thoracentesis and paracentesis. Chest 2013;143:532–8. Peris A, Tutino L, Zagli G, et al. The use of point-of-care bedside lung ultrasound significantly reduces the number of radiographs and computed tomography scans in critically ill patients. Anesth Analg 2010;111:687–92.
Keywords: point-of-care ultrasound; bedside ultrasound; pediatric emergency ultrasound; lung ultrasound; pneumothorax; pneumonia; pleural effusion; alveolar-interstitial syndrome
*Division of Emergency and Transport Medicine, Children's Hospital Los Angeles, Keck School of Medicine/University of Southern California, Los Angeles, CA 90027; †Division of Emergency Medicine, Children's National Medical Center, George Washington University School of Medicine and Health Sciences, Washington, DC. Reprint requests and correspondence: Joshua Sherman, MD, Division of Emergency and Transport Medicine, Children's Hospital Los Angeles, Keck School of Medicine/University of Southern California, Los Angeles, CA 90027. [email protected] (J.M. Sherman), [email protected] (A.M. Abo) 1522-8401 © 2015 Elsevier Inc. All rights reserved.
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Evaluation of Pulmonary Emergencies Using Point-OfCare Ultrasound in the Pediatric Emergency Department: A Review Joshua M. Sherman, MD*, Alyssa M. Abo, MD†
P
oint-of-care ultrasound (POCUS) has a wide array of applications in the pediatric emergency department (ED). Over the past 3 decades, lung ultrasound (LUS) has evolved and become an asset in evaluating both emergent and critically ill patients. Ultrasound (US) of the lung was once thought to be of little utility because normal lung is aerated and US cannot directly visualize air. Thus, it was unclear how US would be beneficial. It is now apparent that US of the chest is extremely useful in evaluating not only normal lung but also pathologic conditions such as pneumothorax, consolidations, interstitial syndromes, and pleural effusions. The key to understanding how LUS works is rooted in US physics and artifacts, and
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specifically, how US waves behave when they encounter an aerated vs pathologic lung.
BACKGROUND Point-of-care transthoracic lung ultrasound (TTLUS) was first developed and proven beneficial in adults and more recently adapted to pediatrics. In emergency and critical care settings, the role of TTLUS has traditionally been used to evaluate pleural effusions and to guide thoracocentesis. 1 However, beginning in the 1980s, there were reports that US could be used to identify patients with pneumothorax 2 as well as pneumonia. 3 Subsequently, in the 1990s, Lichtenstein et al 4 -7 began reporting their findings of bedside LUS in the intensive care unit. These initial studies identified many of the artifacts that are crucial to LUS and laid the foundation of point-of-care LUS. The term artifact is used to explain a by-product of US that is displayed on the screen when sound waves encounter a certain medium, but in reality is not there. In the early 2000s, emergency physicians began publishing data on point-of-care LUS in adults in the ED. Many of the initial studies were related to pneumothorax, and by 2004, Kirkpatrick et al 8 described the evaluation of pneumothorax as part of the trauma evaluation. These data, along with other case reports and studies, 9 -11 ultimately led to incorporating LUS into the focused assessment with sonography in trauma (FAST) examination, which is now termed the extended FAST or EFAST. 12 At the same time, research was underway to understand how LUS could play a part in the diagnosis and management of other disease processes. In 2005, Mathis et al 13 demonstrated its ability to diagnose pulmonary embolism, whereas Reissig and Kroegel 14 showed its utility in diagnosing and following pneumonia in 2007. Transthoracic lung ultrasound has been proven to be useful in adult disease states such as pulmonary embolism, 15 -20 acute respiratory distress syndrome, 21 and acute respiratory failure. 22 In 2012, international evidence-based recommendations for point-of-care LUS, including pediatric data, were published, reinforcing the use of POCUS for lung evaluation in children. 23 Over the past 15 years, research has been published regarding LUS in pediatrics; however, available data mainly address pneumonia and other infectious processes. There is little published research regarding LUS and the diagnosis of pneumothorax in the pediatric population. Therefore, pediatric emergency specialists have incorporated point-of-care
TTLUS in the pediatric population based largely on the literature from the emergency care of adults. This article reviews the clinical utility of pointof-care TTLUS, in pediatric emergency and critical care medicine, in the diagnosis of pneumothorax, lung consolidations, interstitial syndromes, and pleural effusions. The evidence and sonographic findings specific to each of these disease processes will be reviewed, and the future of point-of-care TTLUS in pediatrics will be discussed.
LUNG ULTRASOUND: PRINCIPLES AND TECHNIQUE The advantage of POCUS is multifold. Bedside US can be performed concurrently with the physical examination, expanding the data available to the clinician in real-time, and is rapid and repeatable. Another major advantage is that US does not produce any ionizing radiation. In an era where efforts are made to comply with the ALARA (as low as reasonably achievable) principle regarding radiation exposure, US reduces the radiation exposure for pediatric patients. There are a few disadvantages of which the sonographer should be cognizant. First and foremost, US is operator dependent. Therefore, clinicians must be properly trained in POCUS of the lung and deemed competent before making medical decisions based on the results. In addition, US is unable to visualize pathology below aerated lung; the disease process must extend to the pleura to be identified. Thus, any pathology lying below aerated lung will not be visualized. The key to understanding LUS is based on physics and artifacts. In simple terms, US cannot travel through air without getting scattered and reflected; therefore, when the lung is aerated the sonographer can only visualize the ribs and the pleural surface between the ribs (Figure 1). In older children, the ribs will produce anechoic “black” shadows because the US cannot pass through bone (Figure 1). However, in younger children, the bones are cartilaginous and therefore do not produce the same shadows (Figure 2). Below the pleura is aerated lung, which the sonographer cannot directly see. What can be seen are reflections of the pleural line, which are termed A lines. These A lines are horizontal lines that are a result of sound reverberating or bouncing between the pleura and the transducer; hence, the A lines are equidistant from one another (Figure 1). The pleura between the 2 ribs will give a shimmering effect because of the to-and-fro movement of the 2 layers
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Figure 1. Normal lung, showing the pleura, A lines, and ribs (*).
of the pleura rubbing against one another. This is termed lung sliding and cannot be appreciated in a still image (Video 1). In the case of a pneumothorax, there is no lung sliding. In addition to lung sliding, there are comet tail artifacts that arise from the interface of pleural sliding with air. Small comet tail artifacts called “Z lines” are normal, they fade, and they do not disrupt the A line pattern (Figure 3). To the contrary, “B lines,” which are also a type of comet tail artifact, are abnormal when more than a few are present. They extend from the pleura line to the edge of the screen and do disrupt the A lines (Figure 3). This disruption occurs because of fluid in the lung that allows for the transmission of sound. In addition, B lines move with lung sliding, and they do not fade. Pathology of the lung is evident when the balance of air and fluid within in the lungs changes or when there is an accumulation of air or fluid between the
Figure 2. Lung of a neonate, pleura is visible below the cartilaginous ribs (*).
Figure 3. Comet tail artifacts: Z lines on left compared to a B line on right.
pleural layers as in a pneumothorax or pleural effusion, respectively. As for consolidations and interstitial syndromes, the balance between fluid and air determines what the sonographer visualizes. In interstitial syndromes, there is more air than fluid in the lung, whereas in consolidations, there is more fluid than air. There are varying approaches to interrogating the lungs with US. Lung ultrasound techniques vary. First and foremost, the sonographer must choose an appropriate probe. High-frequency linear probes may be the probe of choice for evaluating the pleura, as their high resolution is ideal for shallow structures; the caveat being that these probes cannot evaluate structures deep in the chest. Highfrequency linear probes are also ideal for evaluating for pneumothorax. If the clinician is concerned about fluid (including interstitial syndromes, pleural effusions, or consolidations), then a phased array or
Figure 4. Base of the lung where the lung meets the diaphragm (= =).
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Figure 5. Right upper quadrant view, mirror image of the liver.
curvilinear probe would be more appropriate. These probes have lower frequency and allow for the evaluation of deeper structures. Once the probe is chosen, the next step is where to place the probe. There are varying approaches on how to evaluate the lung fields. Despite the existence of an international recommendation, there is not one standard accepted way to interrogate the lungs with US. 23 It is generally accepted that if the clinician is concerned for a pneumothorax, the probe should be placed anteriorly on the supine patient. If the concern is for fluid or another gravity-dependent process, then the clinician should interrogate the axillary and posterior lines at the base of the lung where the lung meets the diaphragm (Figure 4). A comprehensive approach, dividing the
chest in 28 zones, has been described; 24 however, division of the chest into 4 to 6 zones on each side is a more reasonable approach in the ED setting. 25 The 6 zones would include a superior and inferior view in the anterior, axillary, and posterior portion of each side of chest (12 views in total). It is also important that clinicians are aware that the lung is visible when evaluating other structures, including the inferior vena cava and the heart in the parasternal view, as well as the upper quadrant views of the FAST examination. These unconventional views can certainly identify pathology that the clinician did not expect. For example, when evaluating the right and left upper quadrants in a trauma evaluation, the area above the diaphragm is normally aerated lung, which provides a mirror image of the solid organ (spleen or liver) (Figure 5) in normal circumstances. In the case of a pleural effusion or consolidation in the chest, the lung is no longer aerated, and the sound is transmitted through the diaphragm and the spine is visualized in the chest. This is termed the spine sign (Figure 6).
APPLICATIONS Pneumothorax One of the most important applications of point-of-care TTLUS in the ED is the evaluation for pneumothorax. This lifesaving application is well studied in adult medicine and takes the provider a few minutes to perform. Answering the question, “does the patient have a pneumothorax?” can drastically change the management of the trauma patient.
Evidence
Figure 6. Spine sign: pathology in the lung allows the transmission of sound; hence, the spine if visible above the level of the diaphragm.
In 2005, Lichtenstein et al 7 published a landmark article on the use of TTLUS for evaluation of pneumothoraces. In a retrospective study spanning 10 years, the authors studied patients who received chest computed tomography (CT), chest radiograph (CXR), and US. They evaluated 43 hemithoraces with radiooccult pneumothoraces against 310 hemithoraces with no pneumothorax. Using US, they evaluated the lung for the following findings: absence of lung sliding, absence of lung sliding with A line sign, and evaluation of a lung point (the junction of normal lung sliding and absent lung sliding). Each examination only took 2 minutes. When the examination revealed absence of lung sliding, LUS had a sensitivity of 100%, specificity of 78%, negative predictive value (NPV) of 100%, and positive predictive value (PPV) of 40%. When combining the absence of lung sliding with the A
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Figure 7. M-mode image—normal lung.
line sign, the modality had sensitivity of 95%, specificity of 94%, NPV of 99%, and PPV of 71%. However, if a lung point was identified, the sensitivity of this study became 79%, and specificity rose to 100%, with NPV of 97% and PPV of 100%. The authors therefore concluded the following: (1) lung sliding rules out pneumothorax; (2) lung point rules
Figure 8. M-mode image—pneumothorax.
in pneumothorax; and (3) LUS for evaluation of pneumothorax has high feasibility, high sensitivity, and rapidity, with a simple technique and a short learning curve. In 2006, Zhang et al 11 evaluated trauma patients in the ED using US to detect pneumothoraces. The study showed that US was more sensitive and more
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Figure 9. Lung pulse on M-mode.
accurate than CXR in detecting pneumothorax. The authors showed that the time needed for diagnosis of pneumothorax was significantly shorter with US compared to CXR (2.3 ± 2.9 vs 19.9 ± 10.3 minutes; P b .001). The diagnostic sensitivity for detecting pneumothorax with US vs radiography was also found to be clinically significant; 86.2% vs 27.6% (P b .001). Ultrasound was highly consistent with CT in determining the size of pneumothorax (κ = 0.669; P b .001). According to the International Consortium for POCUS, 23 LUS should be used in clinical settings when the differential diagnosis includes pneumothorax. They also report strong evidence (level A) to support the statement that LUS more accurately rules out the diagnosis of pneumothorax than supine CXR. A 2014 case series demonstrated the utility of US in guiding needle placement in patients with spontaneous pneumothorax. 26 Future pediatric studies are needed to further evaluate this US-guided procedure.
Sonographic Findings The normal lung is characterized by lung sliding (Video 1). This sliding is a to-and-fro movement visible at the pleural line and is caused by inspiratory excursion of the lung toward the abdomen. If the clinician is unsure whether the lung is sliding, both color Doppler and motion mode can be of assistance. In normal lung, lung sliding will
produce flashes of color along the pleura line (Video 2) that will not be present in patients with pneumothorax. Normal lung also exhibits artifacts known as A lines and comet tail artifacts. In pneumothorax, while A lines persist, lung sliding and comet tail artifacts are absent as the pleural layers are now separated by air. When using motion mode (“M-mode”), normal lung sliding produces an image known as the seashore sign, which is a distinction of 2 patterns: (1) the wave-like pattern above the pleural line and (2) the sand-like pattern below the pleural line (Figure 7). In M-mode, for patients with a pneumothorax, the image will look like a barcode (“barcode sign”) or like the stratosphere (“stratosphere sign”) (Figure 8). The lung point is the transition zone from normal lung to lung affected by a pneumothorax; seashore sign and the barcode are next to each other where normal lung sliding ends and lack of movement begins. It is crucial that the M-mode caliper be placed in the middle of the pleural space. When evaluating a patient for pneumothorax, the sonographer must be familiar with both the false positives and false negatives. False-negative studies are usually those where the examination is incomplete or when there are small apical pneumothoraces that are not detected. False positives, on the other hand, are often cases where the patient has pleural adhesions or a main stem intubation. In the case of a main stem intubation, the lung will not be sliding, but
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Figure 11. Air bronchograms within the lung, a tree-like pattern.
Figure 10. A, Consolidation: Shred sign. B, Consolidations: Hepatization of the lung.
on M-mode, the sonographer may appreciate a lung pulse. The pattern is alternating between seashore and bar code and occurs because the collapsed lung is vibrating in a pulse-like fashion because of the lung's proximity to the beating heart (Figure 9).
which confirmed the presence of pneumonia. In the 3 remaining patients, the clinical course was consistent with pneumonia. Sonographic findings of pneumonia included echogenic areas with illdefined borders and the absence of lung sliding and A lines. Comet tail artifacts were sometimes seen within the consolidation. The investigators also showed that TTLUS is helpful in differentiating among types of consolidations, such as pneumonia and atelectasis, by identifying dynamic air bronchograms within the consolidation. The main limitation of this study was the authors' inability to report on the sensitivity and specificity of TTLUS because chest CT, which one might consider as an imaging criterion standard for pneumonia, was not performed on every patient for obvious ethical reasons. The other limitations were that: (1) no lateral CXR was obtained, only a single anterior-posterior view
Consolidations Evidence In 2008, Copetti and Cattarossi 27 published a landmark article that compared the diagnostic accuracy of point-of-care TTLUS and CXR in children with suspected pneumonia. Seventy-nine children from 6 months to 16 years of age with clinical symptoms of pneumonia such as cough, tachypnea, crackles, and decreased breath sounds were studied. Ultrasound was positive in 60 patients, whereas CXR was positive in 53. Of the 7 patients with a negative CXR and positive US, 4 underwent chest CTs (performed for recurrent pneumonia),
Figure 12. Multiple B lines.
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was taken, and (2) sonography was only performed by one clinician who was an expert in sonography. In 2012, Shah et al 28 increased the sample size and published a study aimed at determining the accuracy of point-of-care TTLUS for the diagnosis of pneumonia in children and young adults. This was a prospective observational cohort study involving 200 patients from 2 different EDs. Ultrasound examinations were performed by 15 different emergency medicine physicians with varying levels of expertise after a 1-hour LUS training session. Children aged 0 to 21 years undergoing a CXR for suspicion of pneumonia were included in the study. In this study, they used CXR as the criterion standard. By visualizing consolidation with sonographic air bronchograms, TTLUS had a sensitivity of 86% and specificity of 89%, with a positive likelihood ratio of 7.8 and a negative likelihood ratio of 0.2. Interestingly, for a subgroup of 187 patients who had a consolidation of greater than 1 cm, the specificity increased to 97% and the positive likelihood ratio to 28, while the negative likelihood ratio decreased to 0.1. The authors concluded that clinicians are able to diagnose pneumonia in children and young adults using POCUS with high specificity. The 2012 International Guidelines published gave very strong recommendations regarding TTLUS for the diagnosis of pneumonia. 23 The authors concluded that LUS is as accurate as CXR in the diagnosis of pneumonia in pediatric patients. Furthermore, LUS for the detection of lung consolidation should be used because it can differentiate consolidations due to pulmonary embolism, pneumonia, or atelectasis, based on visualization of sonographic air bronchograms. It is noted that LUS should be considered an accurate tool in detecting consolidation when compared to CXR. In addition, in mechanically ventilated patients, LUS is more accurate than portable CXR in detection of consolidation. It is important to note that according to this source, LUS does not rule out consolidations that do not reach the pleura. More recently, in 2014, Esposito et al 29 published a prospective observational study regarding the performance of TTLUS in diagnosing community-acquired pneumonia. They included otherwise healthy children aged 1 month to 14 years who were admitted to the hospital with fever and clinical signs and symptoms of community-acquired pneumonia, such as cough, tachypnea, respiratory distress, grunting, wheezing, or rales. Anterior-posterior as well as lateral CXR images were obtained and read by a radiologist. Transthoracic lung ultrasound was performed by pediatric residents who had partici-
pated in a 1-day LUS course. They reported that when compared to CXR, TTLUS had a sensitivity of 97.9% and specificity of 94.5% with a PPV of 94% and an NPV of 98.1%. In addition, TTLUS was found to detect higher numbers of pleural effusions. In 2015, Pereda et al 30 published a meta-analysis of studies involving LUS for the diagnosis of pneumonia in children. They reported LUS as having a sensitivity of 96% and specificity of 93%, with a positive likelihood ratio of 15.3 and a negative likelihood ratio of 0.06. The authors concluded that current evidence does support LUS as an imaging alternative for the diagnosis of childhood pneumonia and advocate for the training of pediatricians in LUS.
Sonographic Findings There are a number of sonographic findings described with consolidations, including the shred sign and the tissue sign. Consolidations of the lung are filled with more fluid than air and therefore are well delineated. These areas are echogenic and are often surrounded by pleural effusions. The shred sign is when the edge of the pleura looks irregular and shredded (Figure 10A); the tissue sign, also referred to as hepatization of the lung, is when the lung begins to look like the liver (Figure 10B). In the latter image, not only does the lung look like liver, but it is surrounded by a pleural effusion, and the spine is visible above the level of the diaphragm. Vertical artifacts can sometimes be seen within the consolidation. These may be comet tail artifacts but are different than B lines as they do not originate at the pleural line but rather from within the consolidation. In addition, air bronchograms may occasionally appear as branching echogenic structures within the consolidation (Figure 11). Dynamic air bronchograms, in which the movement of air with breathing is visible within the consolidation, rule out atelectasis. 31
Alveolar-Interstitial Syndromes Several interstitial disease syndromes can be identified with POCUS. In adult emergency medicine, the most commonly identified interstitial syndrome is pulmonary edema, often seen in patients with congestive heart failure or fluid overload. Other interstitial syndromes include pulmonary contusions, pneumonia, and pneumonitis as well as bronchiolitis, which is more common in pediatrics. The hallmark finding of interstitial syndromes is the B line (Figure 3). In patients with extensive parenchymal disease, US can identify pleural and subpleural abnormalities as well.
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Figure 13. Pleural effusion.
Based on the international evidence-based recommendations, there is strong evidence to suggest that B lines are the sonographic sign of interstitial syndromes. 23 Level A recommendations state that the technique should involve scanning at least 8 regions, with 3 or more B lines in a longitudinal plane between 2 ribs indicating a positive region for interstitial disease. There is strong evidence to suggest that LUS is superior to CXR for diagnosing or excluding a significant interstitial syndrome.
Evidence Bronchiolitis. Caiulo et al 32 published a 2011 study comparing TTLUS with CXR in children aged 1 to 16 months with clinical signs and symptoms of bronchiolitis, based on the American Academy of
Figure 14. Lung edge visible within pleural effusion; positive spine sign.
Pediatrics definition. They used the Downes' Score to categorize the patients into mild, moderate, or severe bronchiolitis. They found that LUS was positive for bronchiolitis in 47 of 52 patients, whereas CXR was positive in 38 of 52 patients and concluded that LUS is a simple and reliable tool for diagnosis of bronchiolitis. The article also describes sonographic findings suggestive of bronchiolitis. However, there were many limitations to this study. As bronchiolitis is a clinical diagnosis, there is no true criterion standard. The American Academy of Pediatrics recommends against the use of routine chest radiography in children with suspected diagnosis of bronchiolitis. 33 Therefore, a “normal” CXR does not exclude the diagnosis of bronchiolitis. Further studies are needed to assess the utility of TTLUS in the diagnosis of bronchiolitis. Pulmonary Contusions. Pulmonary contusions are a possible result of blunt trauma to the chest in both pediatric and adult patients. In 2006, Soldati et al 34 investigated the utility of POCUS in diagnosing pulmonary contusions. Patients were evaluated with LUS initially, followed by CXR and CT scan. Contusions were defined as: 1. Alveolointerstitial syndrome, defined as the presence of multiple B lines arising from the pleural line, in a patient with no clinical suspicion of cardiogenic pulmonary edema. 2. Peripheral parenchymal lesion, defined as the observation of C lines, confluent consolidations (“hepatization”), or parenchymal disruption with localized pleural effusion. Patients were excluded if they had a pneumothorax. The study showed that when alveolointerstitial syndrome was used as the diagnostic criterion for pulmonary contusion, TTLUS sensitivity was 94.6%; specificity, 96.1%; PPV and NPV, 94.6% and 96.1%, respectively; and accuracy was 95.4%. When peripheral parenchymal lesion was used as the criterion, sensitivity and NPV fell to 18.9% and 63%, respectively; however, the specificity and PPV both increased to 100%. A 2009 case report described the use of POCUS in detecting a pulmonary contusion in a pediatric patient after blunt trauma. 35 The contusion was confirmed on chest CT. Future studies are needed in pediatrics regarding POCUS in trauma for both pneumothorax and pulmonary contusions.
Sonographic Findings As discussed previously, normally, the lung is filled with air and does not allow for visualization of normal lung parenchyma. As mentioned, in normal
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Figure 15. M-mode image of a pleural effusion shows a sinusoidal pattern.
lung, A lines are horizontal artifacts that are equidistant from each other, whereas B lines are vertical comet tail artifacts arising from the pleural line, reach the edge of the screen, erasing A lines, and move with normal lung sliding. Multiple B lines are the hallmark of interstitial disease and can be seen in pulmonary edema and pulmonary contusions as well as bronchiolitis. According to Caiulo et al, 32 findings consistent with bronchiolitis include presence of subpleural lung consolidations, defined as subpleural areas with a tissue-like appearance or poor echo structure with blurred margins; presence of compact B lines, defined as areas of white lung; pleural line abnormalities, defined as irregular appearance of pleural line; and the presence of focal areas with numerous B lines (Figure 12).
Pleural Effusion Evidence Lung ultrasound can be used for detecting pleural effusions. Kocijancic et al 36 demonstrated that LUS is more sensitive than lateral decubitus CXR in detection of small pleural effusions. Calder and Owens 37 established that LUS performed better than CT or magnetic resonance imaging in showing septated effusions and/empyemas.
The International Consortium for Point-of-Care Ultrasound reported with strong evidence-based recommendations that: 23 1. A pleural effusion with internal echoes suggest exudate or hemorrhage. 2. For detection of pleural effusion, LUS is more accurate than supine CXR and is as accurate as CT. 3. When a CXR identifies both opacities and effusion, an LUS should be obtained because it is more accurate than CXR in distinguishing between opacities and effusion.
Sonographic Findings In normal lung, the visceral and parietal pleura are in contact with one another; however, when a pleural effusion is present, fluid (usually anechoic) separates the pleural layers (Figure 13). Pleural effusions allow for the visualization of the spine above the diaphragm (Figure 14). On M-mode, if the caliper is placed at the edge of the lung that is surrounded by fluid, this will result in the “sinusoid sign” representing respiratory movement of the lung within the effusion (Figure 15).
FUTURE CONSIDERATIONS Point-of-care LUS has an important role in pediatric emergency medicine. Specific pediatric
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LUS research is crucial to advance the field. Protocols and algorithms would be extremely useful for clinicians and could ensure consistency among providers on how to integrate POCUS into medical decision making. Multicenter bedside US studies would greatly benefit the pediatric emergency medicine community.
SUMMARY It is evident that point-of-care LUS is in an asset in pediatric emergency medicine. Visualizing the lung in real time can aid the clinician in diagnosing pathology as well as assisting with procedures. Point-of-care ultrasound has been shown to decrease complications associated with thoracocentesis. 38 Furthermore, POCUS has been shown to reduce the number of radiographs and CT scans in critically ill adults. 39 If POCUS becomes widely accepted in pediatric emergency medicine, it can reduce the amount radiation to which children are exposed. In the meantime, clinicians with a background in POCUS are encouraged to continue exploring this interesting field of medicine.
ACKNOWLEDGMENTS Conflict of interest: None. Supplementary data (eg. videos) to this article can be found online at http://dx.doi.org/10.1016/j.cpem.2015.11.006.
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