(Chest. 2002;122:1759-1773.)
© 2002
American College of Chest Physicians
Real-Time Chest Ultrasonography*
A Comprehensive Review for the Pulmonologist
Sonja Beckh, MD;
Pál L. Bölcskei, MD and
Klaus-Dieter Lessnau, MD, FCCP
* From the Department of Pulmonary Sonography (Dr. Beckh), Division of Pulmonary Medicine (Dr. Bölcskei), Center of Internal Medicine, Nuremberg, Germany; and Department of Respiratory Care Services (Dr. Lessnau), Division of Pulmonary and Critical Care Medicine, Lenox Hill Hospital, New York, NY.
Correspondence to: Klaus-Dieter Lessnau, MD, FCCP, 300 E 93rd St, No. 18B, New York, NY 10128; e-mail: KLessnau{at}pol.net
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Abstract
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This review discusses real-time pulmonary ultrasonography (US) for the practicing pulmonologist. US supplements chest radiography and chest CT scanning. Major advantages include bedside availability, absence of radiation, and guided aspiration of fluid-filled areas and solid tumors. Pulmonary vessels and vascular supply of consolidations may be visualized without contrast. US may help to diagnose conditions such as pneumothorax, hemothorax, pleural or pericardial effusion, pneumonia, and pulmonary embolism in the critically ill patient who is in need of bedside diagnostic testing. The technique of US, which is cost-effective compared to CT scanning and MRI, may be learned relatively easily by the pulmonologist.
Key Words: critical care medicine • pulmonary medicine • review • ultrasonography
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Introduction
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During the past 20 years, new techniques have emerged in thoracic imaging, such as spiral CT scanning, high-resolution CT scanning, and MRI. The ability to transform images into electronic data that may be manipulated and shared with other consultants has revolutionized health care.1
2
Real-time ultrasound (US) has shown to be useful in the diagnosis and treatment of patients with pulmonary diseases. This review describes the clinical application of real-time US in pulmonary and critical care medicine with clinical examples and compares its use to those of other imaging techniques.
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Technical Equipment
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Visualization of the chest wall requires a higher frequency linear probe (5 to 7.5 MHz), whereas pleural and pulmonary pathology is better detected with a sector or phased array probe with lower frequency (3.5 MHz).3
4
A convex array probe (3.5 to 5 MHz) combines the advantage of adequate close resolution and the ability to access deeper structures between the ribs. All described examinations were performed by a pulmonologist. Recently developed, and still expensive, devices having high-frequency probes (10 to 13 MHz) provide excellent resolution, more contrast in gray scales, and color Doppler angiography with the detection of very small vessels. However, there are an insufficient number of published studies to prove the clinical benefits of using these new devices at this time. Therefore, these devices will not be discussed in this review.
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The Technique of US Examination
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To examine anterior and posterior parts of the chest, the patient should be in a sitting position with arms elevated and hands clasped behind the neck (Fig 1
). Even with this technique, some parts of the upper lobes remain hidden behind the scapulae. Pleural movement is observed during inspiration and expiration. Solid lesions close to the diaphragm require special maneuvers, such as sniffing or coughing. The probe may be moved in longitudinal and transverse directions to visualize the lung surface through the intercostal spaces, thereby avoiding the ribs. The patient also may lie in the prone, supine, or lateral positions. Caudal parts of the lung may be examined from an abdominal view. The right lung is visualized through an abdominal window, passing through the liver and diaphragm, and the left lung is visualized by passing through the spleen and diaphragm.
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Indications for Sonographic Imaging
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Chest Wall
Numerous studies5
6
7
evaluating US chest wall imaging have been published. The visibility of muscle and bone has steadily increased with equipment advances (Table 1
). Different parts of the chest wall may now be well-delineated with current techniques (Fig 1)
. The margins of normal ribs are outlined as uninterrupted echogenicities similar to normal pleura, while the pleura is moving continuously during respiration. The US beam passes through cartilage better than through muscular tissue. Therefore, the pleural line appears slightly curved behind the cartilaginous part of ribs. This should not be interpreted as a pathologic condition.
Chest Pain From Benign Lesions
A patient might consult a pulmonologist to evaluate chest pain after trauma. The transducer is placed over the area of pain and is moved slightly. Figure 2
shows the broken rib of a young woman who had fallen onto the sharp edge of a sidewalk 1 day earlier. The US beam passes through dislocated bone and is reflected by the lung surface, producing reverberation artifacts, or the "chimney phenomenon."3
4
Hematomas around fractures are characterized as an echo-poor or dull areas surrounded by soft tissue. US may provide a rapid diagnosis, even in patients with chronic obstructive lung disease and osteoporosis, in whom sudden painful rib fractures may occur as result of coughing. US may be superior to chest radiography and equivalent to rib radiographs, CT scanning, and MRI in the diagnosis of rib fractures.3
4
Chest pain may occur without an obvious cause. A 69-year-old man with a history of right-sided thoracoplasty for tuberculosis in 1955 had right-sided chest pain and swelling below the right clavicle. A US examination utilizing a 7.5-MHz probe demonstrated a small duct, originating from the thoracic cavity and extending into muscles (Fig 3
), through which slowly moving tiny dots could be seen. Thoracentesis revealed a yellow oily liquid representing a rupture of the oil plombage, which had been utilized 44 years earlier for the treatment of cavitary tuberculosis. A chest CT scan had not detected this fistula.
Chest Pain From Malignant Lesions
Malignant infiltration of muscle, bone, or parietal pleura may cause pain early in the course of disease. Changes or destruction may be visualized, and its extension may be measured. A 66-year-old woman complained of left lateral chest pain. She recalled a fall from a staircase 6 months earlier, and pain had continued since that time. A CT scan revealed swelling around the third and fourth rib, which was thought to be an old hematoma adjacent to the fractured ribs. Ultrasonographic imaging (Fig 4
) revealed a malignant tumor, infiltrating from the pleural space into the muscles and the ribs. Suzuki et al8
and Sugama et al9
have reported an accuracy of 100% with US for tumor invasion of the chest wall. Both studies compared preoperative findings with surgical results in 185 patients. The utility of US in the diagnosis of malignant invasion of soft tissue may exceed that of CT scanning, which had a specificity of only 68% in one study.8
Despite the advantages of US, malignant diseases of the chest require chest radiography and CT scanning to evaluate the entire thorax.10
Lesions close to the vertebrae are difficult to detect by US alone. Rapoport et al11
described superior imaging of the brachial plexus by MRI. Padovani et al12
found MRI to be useful in the diagnosis of apical tumors. Arcasoy and Jett13
described MRI as being superior to CT scanning in the identification of chest wall invasion and in determining the extension of a tumor into the brachial plexus, vertebral bodies, spinal cord, and subclavian vessels. However, the usefulness of US was not studied in these reviews.
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Pleural Diseases
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Normal US Findings
Less than 1 mm of space is usually present between the parietal and visceral pleura. A thin echogenic lining represents parietal pleura. The visceral pleura may be slightly blurred due to reflection artifacts from the US beam as it encounters a lung surface. Both pleural surfaces may rarely be visualized on standard US pictures. However, the parietal pleura does not move, whereas the visceral pleura moves with respiration.
Pleural Effusion
US imaging is the best method for diagnosing pleural effusion and differentiating pleural fluid and pleural thickening.14
15
16
Pleural effusion is easily detected by US as an echo-free or dark zone. The changing shape of the lung may be observed when compressed by fluid (Fig 5
). The first step is to determine whether the effusion is transudate or exudate. Transudates have an echo-free pattern, although partially treated transudates of congestive heart failure may occasionally be echogenic.17
Small moving dots in an effusion indicate leukocytes, erythrocytes, fibrin, or protein particles. Inflammatory pleural diseases produce exudates that contain fibrous strings and mobile or immobile septations with encapsulated liquid.4
17
18
Several formulas exist for estimating the volume of the effusion. A useful technique for clinical purposes is to measure the maximal lateral and posterior height of the effusion in centimeters and then to multiply by 90 (ie, the prediction error for 300 mL; r = 0.68). The maximal height is added to the maximal distance from the basal lung parts to the diaphragm, and the sum is multiplied by 70 (ie, prediction error for 200 mL; r = 0.87).17
Thoracentesis and biopsy of the parietal pleura may be required for diagnosis.19
20
21
22
Although US is a safe method for both procedures,23
it may not always be useful. Hypoechoic lesions may be misinterpreted as encapsulated fluid. Occasionally, the needle may deviate from the area of interest and penetrate into deeper intrathoracic regions.17
Pleural Thickening
Pleural thickening is seen as a peel of tissue accompanying pleurisy or empyema. Calcification may be detected with old tuberculosis. Benign cases of pleural thickening do not infiltrate the chest wall and ribs, and demarcate against the aerated lung. Color Doppler US is useful in differentiating fluid from solid parts. In a study by Wu et al,24
33 of 35 patients with pleural effusions had colored images, whereas 16 patients with pleural thickening did not have colored images. Fluid in the pleural space relates to breathing and cardiac contractions. Any movement of body fluid may be translated into colored images. Pleural thickening has no movable parts, and colored signals may not be detected.
Pleural Malignancy
Neoplasms of the pleura are rare, except for malignant pleural mesothelioma.25
Figure 6
is the image of a pleural lipoma found incidentally on a routine chest radiograph. The lung is moving freely along the smooth-edged tumor, which is based on the parietal pleura, producing an echogenic pattern on real-time US. A CT scan helped to diagnose the lesion by revealing the typical low fat-like density. Tumor infiltration may present as diffuse or occasionally as irregular parietal pleural thickening (Fig 7
). Metastatic nodules may be detected on the parietal and diaphragmatic pleura. These nodules are echogenic, may be round or polypoid, and are well-demarcated against the surrounding tissue or pleural fluid.17
The combined findings of pleural fluid and nodules, or sheet-like thickening, in a patient with a known primary malignancy, are highly suggestive of metastatic disease.26
27
Pleural carcinomatosis may not be detected by US imaging in patients with malignant effusions due to the small size of the tumor seeding.17
Carcinomatosis of the visceral pleura is more difficult to detect by US because of reflection artifacts of the lung surface. It may be impossible to distinguish pleural carcinomatosis and peripheral lung carcinoma. A US-guided core-needle biopsy is very accurate28
in diagnosing malignant pleural mesothelioma (Fig 8
).
The Diaphragmatic Pleura
The entire right hemidiaphragm is visualized by US because the liver fills the dome completely, allowing excellent transmission of the beam. The left acoustic window is smaller because the spleen attaches to only half of the hemidiaphragm. Nevertheless, respiratory movements of both hemidiaphragms may always be examined, and diaphragmatic elevation or paralysis may be diagnosed clearly by real-time US without fluoroscopy. Another US application is for the measurement of diaphragmatic thickness and its change during respiration.29
Diaphragmatic furrowing, that is, modeling the cranial surface of the liver, may be visualized in patients with emphysema and COPD. Measurements may be useful with weaning problems, with myodystrophy, and in decision making about the need for permanent assisted ventilation. However, no clinical studies on the utility of US for these conditions are available so far. Infiltration of the diaphragmatic pleura by malignant disease may be observed (eg, Fig 8
), because the diaphragm is irregular and indented by the penetrating neoplasm. Metastases to the diaphragmatic pleura are often nodule-shaped.27
30
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Comparison of US With Other Imaging Methods
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US is more sensitive than posterior-anterior and lateral chest radiographs in detecting small amounts of pleural fluid.31
Pleural fluid is even more difficult to discern on radiographs taken with the patient in the supine position.17
32
On decubital chest radiographs, the differentiation between atelectasis and effusion is occasionally difficult. US better estimates the volume of effusion than radiography.32
US is useful to evaluate pleural opacities by differentiating atelectasis, effusion, and solid or liquid pleural parts. It is the preferred method for image-guided thoracentesis or for the placement of chest tubes. Despite the obvious advantages of US, complementary imaging is mandatory. CT scanning shows the parenchyma, the hilar regions, and the entire surface of the visceral and mediastinal pleura.33
Video-assisted thoracoscopy (VATS) offers the best results for histology of pleural effusion,34
and the technique of semiflexible thoracofiberscopy has been introduced.35
The presence of pleural adhesions prior to surgery may determine the operative choice for thoracotomy or VATS. In the presence of thick, vascularized adhesions, access to the pleural space may be hazardous or impossible with the video thoracoscope. CT scanning was of only moderate utility (sensitivity, 71%; specificity, 72%) in predicting adhesions in a study of 63 patients.36
Contrast-enhanced CT scanning demonstrated vascularized adhesions only poorly (9%). The utility of preoperative US of the pleura to guide VATS and thoracotomy requires further study. CT scanning and MRI are useful in detecting mediastinal and diaphragmatic invasion by malignant pleural mesothelioma.37
Layer et al38
compared CT scanning, MRI, and US in one study. They concluded that CT scanning is preferred for preoperative evaluation, with MRI being of nearly the same value. US is useful in detecting pericardial or diaphragmatic infiltration.
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Pulmonary Embolism
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A variety of imaging techniques for patients with pulmonary embolism (PE) has been studied. The first step in the diagnosis is the chest radiograph. It shows infiltrates, atelectasis, and effusions.39
Ventilation-perfusion scintigraphy is the next step in many institutions. However, the investigators in the Prospective Investigation of Pulmonary Embolism Diagnosis study40
found that only a minority of patients with PE had high-probability scans (sensitivity, 41%; specificity, 97%). One hundred five of 322 patients (33%) with intermediate-probability scans and pulmonary angiograms had PEs. PEs were present in 12% of patients with low-probability scans.40
A new diagnostic tool was introduced with CT angiography, which is a powerful alternative within second to fourth division pulmonary arteries.41
Additional findings42
have revealed characteristic consolidations in patients with acute PEs. Spiral CT scanning has a sensitivity and specificity of 90% in depicting thrombi within the central pulmonary vessels.43
44
45
Nevertheless, the interpretation of CT angiograms was incorrect or indeterminate in 943
to 12%44
of patients. Breathing artifacts may be eliminated by using electron-beam CT scanning,46
which does not require breath-holding during scanning. Contrast pulmonary angiography still remains the "gold standard."47
Meyerovitz et al48
concluded that pulmonary angiography remains the definite test for small subsegmental PEs in a study of 365 pulmonary arteriograms, with 62 having been performed in patients with negative findings on lower extremity sonograms and low-probability perfusion scans. Meaney et al49
found MRI highly accurate in detecting PEs, and it may be more widely used as an alternative to pulmonary angiography.50
Despite their usefulness, critically ill patients may not tolerate any of these procedures. Occasionally, the appropriate equipment may not be available. In such cases, the clinician must base the diagnosis of PE on clinical suspicion supplemented by indirect evidence.51
Bedside US has been used for many years and can demonstrate abnormalities in approximately 40% of patients with PEs.51
Examination of deep-vein thrombosis with US is now widely established.52
The wedge-shaped consolidation of a PE is visualized by CT scanning and also may be seen by US. Infarcted and nonaerated areas of lung parenchyma allow the transmission of the US beam. New pulmonary infarctions are characterized as triangular or wedge-shaped homogeneous hypoechoic lesions with or without effusions.53
54
55
Infarctions detected by US are smaller than perfusion defects due to blurred demarcations against the ventilated normal parenchyma. Older infarcts are better demarcated and show hyperechoic reflexes in the center, representing an occluded bronchiole.54
US examination had a sensitivity of 98% and a specificity of 66% in a study of 58 consecutive patients suspected of having PEs.56
The lower specificity may be explained by consolidation due to other causes that have similar ultrasonographic appearances. US was compared to CT angiography in a study of 117 patients with clinical suspicion of PE.57
Seventy patients had documented PEs. The sensitivity and specificity for US was calculated as 94% and 87%, respectively, and for spiral CT scanning, 85% and 100%, respectively. A 31-year-old woman was admitted to the hospital with sudden onset of left-sided chest pain 6 weeks postpartum. Chest radiograph showed a small pleural effusion. A diagnosis of PE was suspected. However, contrast examinations and scintigraphy were relatively contraindicated since she was breast-feeding. US revealed two typical infarction lesions of the left lower lobe (Fig 9
), accompanied by a small effusion. US also revealed partial thrombosis of the left pelvic vein. US may detect small peripheral emboli, which may go undetected by ventilation-perfusion scintigraphy, whereas large emboli may not be detected by US.53
However, small emboli may precede larger emboli and may predict life-threatening complications. The clinical course of a PE depends on early diagnosis and appropriate treatment.58
US examination may be useful in patients with presumed PE, as well as in patients who are pregnant or lactating and who have negative findings on scintigrams, undiagnosed chest pain, allergies to contrast material, or who may not tolerate transport for other imaging studies. US is cost-effective when performed prior to more expensive procedures.52
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Pulmonary Consolidations
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Pneumonia
Peripheral pulmonary lesions that extend into the visceral pleura may be visualized by US. US differentiates atelectasis and effusion when opacities are present. Inflamed lung parenchyma shows hypoechoic consolidation with blurred margins. The echo-texture is homogeneous and occasionally mimics lung parenchyma, with multiple lentil-sized air inlets.59
60
Echo-texture varies with ventilation. It is heterogeneous with ventilation or homogeneous with small or absent air inlets. The air bronchogram is a typical US sign of pneumonia.61
Air-filled bronchi produce highly reflective echogenic lines within the consolidated parenchyma. With increased ventilation and decreased consolidation, artifacts from the well-aerated lung produce hazy images. In combination with Doppler techniques, new diagnostic approaches with US are possible (eg, lung sequestration was confirmed by examining the abnormal vessel and analyzing blood flow).62
Occasionally, pneumonia may mimic bronchogenic carcinoma. A 37-year-old man had a sudden onset of high fever and cough. He received a diagnosis of pneumonia. A CT scan showed a solid tumor of the thoracic space penetrating into the chest wall. US revealed typical infiltration of the right lower lobe with an echo-poor mass extending from the lung into the muscles (Fig 10
). While the lesion was vascular, it had the typical vascular pattern of a normal lung. Carcinoma was unlikely. A US-guided biopsy with a 21-gauge needle revealed inflammatory cells and no malignant cells. Investigation of a specimen from an open-lung biopsy established actinomycosis. The diagnosis of actinomycosis or nocardiasis is often only made by the examination of resected lung tissue.63
Actinomyces are strictly anaerobic and will not grow in an oxygen environment. Cytologic samples or small tissue biopsies may not be appropriate specimens for keeping organisms viable until delivery to the laboratory.
Abscess and Empyema
A pulmonary abscess may occur in the peripheral lung. US-guided transthoracic aspiration64
or drainage59
60
65
are useful techniques in the diagnosis of abscess and empyema. A variety of echo patterns may be present with empyema. In a study of 320 cases of pleural effusions, Yang et al66
found empyema as homogeneously echogenic. In most cases, septations and multiple moving and swirling reflections correlate with increased protein or cells. However, empyema may occasionally appear echo-poor, as shown in Figure 11
. Thickened walls surround empyema. Using real-time US, the contiguous lung parenchyma usually is fixed to the inflamed areas. The US findings may be important for decision making about treatment and in reducing hospitalization.67
68
In a study by Ramnath et al,67
the group of patients with nonorganized empyema had the same duration of hospital stay, regardless of whether they had been treated with tube thoracostomy or operation. But in the case of patients with septations and loculations, a significant difference was found. These patients did not benefit from drainage procedures, whereas decortication shortened hospitalization. A CT scan helps to distinguish between abscess and empyema.69
70
With lobulated empyema, the CT scan reveals the entire spatial extent. CT-guided drainage69
is performed if ultrasonographic access is not feasible.
Diffuse Interstitial Lung Disease
US does not diagnose diffuse interstitial lung disease, although it may appear as indeterminate scars or irregular artifacts of the lung surface. Thin-section or high-resolution CT scanning is the method of choice,71
72
73
identifying disease to a better degree as normal chest radiographs and outlining abnormalities more extensively than chest radiography.74
Solid Formations
Many peripheral lung lesions, such as those from pneumonia, embolism, metastasis, or primary bronchogenic carcinoma have the same echo-poor appearance on initial US examination. Repeated examinations usually demonstrate changes with inflammatory diseases, whereas malignant lesions do not change their pattern within days. Moreover, benign acute disorders present with a different clinical picture. Differentiating chronic benign infiltrations from malignant consolidations remains difficult and requires further invasive testing.
Metastasis
CT scanning75
and spiral CT scanning76
are the most accurate imaging methods with which to detect small nodules of the entire lung. In a patient with a history of underlying malignancy, one or more nodules may represent metastases.77
US is not particularly useful in detecting metastasis of the lung parenchyma because it offers only limited views. However, it is useful for the biopsy of a peripheral lung lesion. Pulmonary metastases usually appear as echo-poor, round, and well-demarcated lesions. Infiltration of the chest wall may clearly be excluded by observing the gliding of the visceral and parietal pleura.
Primary Lung Carcinoma
The main decision making about peripheral consolidation is differentiating between benign and malignant disease. US may provide useful information. Since many peripheral solid carcinomas do not contain aerated lung parenchyma, US will reveal only small reverberations within the transition to the ventilated normal lung. The infiltrative growth of solid tissue without regard to anatomic structures is characteristic of malignancy. Only rare inflammatory diseases, such as actinomycosis or nocardiosis, spread in this manner. Figure 12
illustrates a large tumor of the left lung extending into the chest wall and mediastinum. Usually, the echogenicity of malignant lesions is homogeneous. Malignancy with surrounding effusion is characterized by an uneven knobby or tuberous surface. A lung consolidated by malignancy moves stiffly and does not change its shape during respiration. Chronic pneumonia may present the same way, although the lung surface always remains smooth. Occasionally, small invading branches of malignant tissue may be detected. Another sign of malignancy is the presence of tortuous vessels. Depending on its extension within the lung parenchyma, bronchoalveolar carcinoma may have a distinct appearance. Consolidated forms resemble pneumonia with blurred margins and air bronchograms, while diffuse infiltrating forms are characterized by rough visceral pleura and grainy subpleural echoes. Benign and malignant lung lesions may be differentiated by their vascular pattern and blood flow using color Doppler US.78
79
80
81
82
However, this procedure has limitations, as some pulmonary vessels are too small for blood flow to be detected. Central malignant tumors may be visualized, if accompanied by atelectasis or obstructive pneumonia of the affected lobe. US shows fluid-filled bronchograms in the consolidated lung of obstructive pneumonia.83
US is an additional tool in the diagnosis of bronchogenic carcinoma. Staging is always performed with CT scanning, and the use of MRI may occasionally be necessary in demonstrating mediastinal lymphadenopathy and in visualizing the entire chest and spine. In determining the operative choice between VATS and thoracotomy, the surgeon may want more information about consolidation. Invasion of the parietal pleura guides operative management.84
Vascular adhesions may increase the risk of bleeding with VATS.85
CT scanning performed during deep inspiration and expiration is effective in outlining tumor invasion in the area of the middle and lower lobes.86
This maneuver is less accurate with the upper lobe because of diminished respiratory movements. Real-time US may observe the gliding of the visceral pleura. The patient is instructed to cough and to sniff in order to observe movements of the upper lobes. However, adhesion or infiltration of the mediastinal pleura cannot always be determined with US, CT scanning, or MRI. At present, no imaging method is particularly useful in this situation, and VATS or explorative thoracotomy is necessary. US may add useful information in the staging of bronchogenic carcinoma. Supraclavicular lymph nodes may be missed by palpation,87
particularly in patients with emphysema. CT scanning may fail to detect these lymph nodes if the cuts start with the apical lung field. Figure 13
illustrates a supraclavicular lymph node that was not detected by palpation or CT scanning.
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Transthoracic US of the Mediastinum
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The most common disorders of the mediastinum in adults are metastasis and primary malignancy. Benign disorders, such as cysts, thymomas, or lipomas, are rare.88
89
The imaging technique designated for evaluating the mediastinum is chest radiography, followed by CT scanning. Although an adequate view of the mediastinum is somewhat impaired by bone, US plays a useful role. In 1971, Goldberg90
first described suprasternal US of the mediastinum. Cardiologists used this access to examine the aortic valve and thoracic aorta.91
92
93
In 1986, Wernecke et al94
described the diagnostic evaluation of mediastinal tumors utilizing suprasternal US. In 1990, he studied mediastinal sonography US with an additional parasternal access.95
He concluded that the sensitivity of US was similar to CT scanning for the supra-aortic, pericardial, prevascular, and paratracheal areas. CT scanning was superior to US for the aortopulmonary window, the subcarinal and paravertebral regions, and the posterior mediastinum. MRI is necessary for evaluating the tumor involvement of vessels, vertebral bodies, or spinal foramina.96
US contributes to the evaluation of the mediastinum despite limited views. Lesions of the anterior superior mediastinum may be identified clearly by US as solid or cystic.96
Tumors that appear at the margin of the sternum are easily localized and biopsied. Guided biopsies minimize the risk of bleeding because the surrounding vessels or tumor vessels are easily evaluated during the procedure without radiation or contrast.97
98
US examination may demonstrate regression after the treatment of mediastinal lymphoma.99
Nevertheless, CT scanning is always necessary for initial staging and for the planning of therapy.100
Superior vena cava syndrome is a complication of bronchogenic carcinoma, and US is a first-line imaging technique with which to evaluate the superior vena cava and adjacent veins. Color Doppler US may detect collateral vessels and small vessels that have not been identified by CT scanning.101
Although echocardiography is usually not performed by the pulmonologist, pericardial effusion is easily diagnosed. A left sternal or subcostal approach provides a nearly echo-free window to the fluid surrounding the myocardium. It might even be possible to diagnose scimitar syndrome by color US. US of the mediastinum has several limitations. Successful examination requires considerable experience in US and visual interpretation, and a thorough knowledge of anatomic structures. Lesions that are located deeper in the mediastinum absorb more US energy and may not be identified against surrounding tissue. Patients with emphysema have reduced suprasternal, parasternal, and aortopulmonary windows that limit US evaluation. Endoscopic US using the flexible bronchoscope is another method with which to evaluate the mediastinal, paratracheal, and subcarinal lymph nodes.102
103
It may be combined with fine-needle aspiration104
or biopsy105
for obtaining cytologic or histologic samples.
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US-Guided Biopsy
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For many years, pulmonologists were limited to the use of fluoroscopy-guided transthoracic biopsies. The introduction of CT scanning in the 1980s allowed clinicians to increase the range of biopsies. Real-time US-guided biopsy of the chest wall or pleural lesions has been performed for years.106
Encouraging results for chest wall lesions,107
108
pleural lesions,109
pulmonary lesions,110
111
and mediastinal lesions112
113
114
have been reported. US-guided aspiration biopsy is successful with peripheral pulmonary nodules smaller than 3 cm115
and lung consolidations with necrotic centers.116
The diagnostic yield for US-guided biopsies ranges between 60% and 100% for definitive cytology and histology in benign and malignant lesions.28
98
106
107
108
109
110
111
112
113
114
115
116
117
118
A 1999 study reported that US-guided biopsy of thoracic lesions is gaining acceptance among radiologists in the US.117
US may easily localize lesions of the chest wall and pleura. Mediastinal masses are only reached by percutaneous US biopsy if they are located anteriorly. Consolidations of bronchogenic carcinoma are often located paratracheally or below the bifurcation. A bronchoscopic transbronchial CT-guided biopsy may be necessary for cytologic or histologic diagnosis.119
Depending on the examiner’s skill and the availability of equipment, transbronchial-endobronchial, US-guided,120
or transesophageal endoscopic US-guided biopsy121
may be performed before using more invasive procedures such as mediastinoscopy. CT scanning of the thorax is always necessary when malignancy of the chest is suspected. However, US may be superior to CT scanning for comparable regions of the chest, with the exception of intrapulmonary lesions that are only visible by CT scanning.118
The advantages of US include the ability to scan variable layers and to visualize lung movement during respiration and needle location during biopsy. Consolidations may be biopsied, while distinguishing solid, liquid, and necrotic areas. Aerated lung parenchyma or large vessels are avoided, allowing safe needle access to the area of interest. The disadvantages of US bear mentioning. A peripheral lesion is undetectable by US with even a very thin layer of aerated lung parenchyma. If a pneumothorax occurs during the biopsy, the lesion will disappear immediately and the procedure must be terminated. Generally, it is safer to biopsy thick-walled cavities than thin-walled cavities.
Performing US-Guided Biopsy
Selection for US-guided biopsy includes patients who will benefit from the result. Severe emphysema and severe pulmonary hypertension, while not absolute contraindications, increase the risks of thoracic biopsies. However, US decreases the risk of injuring the visceral pleura and vessels. The biopsy may be performed in a sitting position if the patient is unable to lie down. The patient should be placed in a position that will prevent sudden movement of the chest. The area of the planned biopsy is cleaned with disinfecting solution that may be used as the transmitting medium instead of the nonsterile sono-gel. Any solution may be used as long as it does not destroy the surface of the relatively expensive transducer. Three different biopsy methods are available, depending on the skill and experience of the practitioner. First, the depth of the lesion is measured. The biopsy needle then may be advanced without US guidance, requiring the pulmonologist to recall accurately the direction and length. This method is recommended for large lesions that have adhered to the parietal pleura or chest wall. Pulmonary, mediastinal, or smaller lesions should be biopsied under US guidance. Using this method, the convex, sector, or linear array is longitudinally placed in the intercostal space of the area to be biopsied. The needle is guided from the margin of the transducer in an oblique axis into the sound area. The third option is the easiest to perform. A special transducer probe with a notch in the middle allows the insertion of the needle in a fixed direction. This permits a safe and accurate biopsy. The cost of this special probe is disadvantageous. However, it may be used for other percutaneous biopsies, particularly those of the abdomen. Special attachments for the transducer cannot be recommended. In addition to their high cost, they are not useful for thoracic biopsies. Their use in the narrow intercostal space may cause the needle to be misguided into a rib. In addition, they make it more difficult to change direction with deep lesions, and they do not provide adequate access with superficial consolidation. The choice of the needle is important for a successful biopsy. Cytologic diagnosis may be obtained with small 19- to 22-gauge aspiration biopsy needles that yield sufficient material. The accuracy for malignant cells is acceptable,122
especially with bronchogenic carcinoma, when cytology fine-needle biopsy is usually diagnostic.123
An adequate histologic specimen is required for benign consolidations, mediastinal masses, and some malignancies, such as lymphomas and sarcomas. Histologic specimens may be obtained with a larger core-needle biopsy or a cutting needle system.123
124
125
126
127
An 18-gauge needle is usually necessary. Modifications of the needle (Tru-Cut; Medex; Towson, MD) with a spring-loaded mechanism or an automatic tissue-sampling biopsy instrument allow the practitioner to perform the biopsy with one hand while the other hand holds the transducer. This approach is safest when one performs the biopsy while observing the needle direction. Local anesthesia should be applied to the biopsy site. Anxious patients may require mild sedation, but cooperation with breathing is necessary for pulmonary lesions.
Complications of US-Guided Biopsies
US-guided biopsies are safe and accurate when performed correctly and have a low complication rate.107
108
109
110
111
112
114
115
116
117
118
Pneumothorax occurs in 1 to 3% of patients, and < 1% will require a chest tube. Bleeding or hemoptysis occurs in 0 to 2% of patients. The complication rate with CT scan biopsies is higher due to the passage through aerated lung. Pneumothorax may occur in up to 24 to 45% of patients, and hemorrhage and hemoptysis may occur in 2 to 10% of patients.117
123
126
128
The technique of coaxial CT biopsy, in which the needle remains in the lesion for repeated biopsies, also carries a higher complication rate. This significant difference is explained with the nonvisualization of intraparenchymal lesions by US. The complication rate between CT scanning and US is not different for biopsies of the same accessible areas that attach to the pleura.118
A study of fluoroscopy-guided needle aspiration of parenchymal lung masses showed significant reduction of the rate of pneumothorax if positional corrections and activity restrictions were applied after biopsy.129
One method is to ask the patient to lie on the biopsy site for 2 h. A chest radiograph is ordered about 4 h later if the aerated lung may have been injured or if dyspnea or pain occurs. Treatment options for iatrogenic pneumothorax include outpatient treatment130
or percutaneous catheter aspiration,131
as an alternative to chest tube insertion and hospitalization. There is a risk of new metastasis in the biopsy channel as result of the biopsy. In 1995, 95,070 US-guided biopsies were reviewed.132
Six metastases (0.0063%) were detected within the biopsy channel after patients underwent fine-needle biopsy. Metastases to the chest wall occurred after large cutting-needle biopsies or after chest tube insertion in 11 cases (0.012%). Metastasis typically occurred with severe and progressive disease. While local metastasis may cause pain, it is not known to decrease life expectancy in patients with carcinoma.
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US in the ICU
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Bedside US offers many possibilities in the ICU setting. Critically ill patients receiving positive-pressure ventilation may develop life-threatening complications during transport or during positioning in the CT scanning or MRI suite. Rapid diagnosis is crucial in deteriorating patients and in acute emergencies. US is invaluable for the immediate detection of pericardial or pleural effusions. The differential diagnosis of pleural fluid may be easily achieved133
(eg, hemothorax simulating liver parenchyma). US is an imaging mode for thoracentesis and chest tube placement in the ICU patient.133
134
US may occasionally detect basal pneumonia in a ventilated patient, which may not be visualized on a supine chest radiograph. Examination from the abdomen through the liver or spleen is useful. However, ventilator-associated pneumonia and atelectasis appear similar on US images and are not distinguishable. With real-time US, the movement of the diaphragm may be observed,133
and reduced motion or paralysis may be of diagnostic value. Patients receiving positive-pressure ventilation with sudden respiratory distress may have tension pneumothorax. US allows rapid diagnosis. Usually, the hyperechoic lung surface may be seen moving, which is known as gliding sign135
or lung sliding.136
The lack of backward and forward movements and of augmented reverberation artifacts suggest air in the pleural space. The size of the lung collapse cannot be determined in the absence of pleural fluid. However, it is possible to describe the area of pneumothorax. For complete evaluation, chest radiography or CT scanning is necessary. In the case of hydropneumothorax, US visualizes the collapsed lung within the fluid.137
An examination of suspected pneumothorax is best performed with a 5 to 7-MHz linear transducer that offers close-area resolution. A 3.5 or 5 MHz convex array may permit sufficient detail as well. US also may be performed after pneumothorax has occurred in order to place a chest tube or to verify that the lung has expanded. With US, the patient may be examined in any position, although movements of the apical lung areas are difficult to detect. US does not detect a localized pneumothorax of the mediastinum. As a rule, CT is necessary to make such a diagnosis, for example, in patients with status asthmaticus.
After the patient undergoes a biopsy or has a central venous line inserted, US gives rapid information about possible complications or line placement. False-positive results for pneumothorax may occur in cases of pleural symphysis (ie, adherence of the parietal and visceral pleura), extensive pneumonia, acute fibrosis, or ARDS.136
The authors explained this with a loss of lung expansion during respiration. The subclavian vein is difficult to image by US. Sector probes with 3 to 5 MHz, using the supraclavicular approach, may work the best. Unfortunately, it is difficult to locate the vessel with the infraclavicular approach. To our knowledge, there are no studies that have evaluated the accuracy of US in imaging these vessels. US has been used successfully to distinguish between pulmonary edema and exacerbation of COPD.138
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Summary
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New imaging techniques have considerably improved the diagnostic and therapeutic capabilities of the pulmonologist.139
US has a valuable role, yet, it is operator-dependent, and training is required. It is a supplement for areas requiring more detailed views. Bedside availability and the absence of radiation allow more patients to be suitable candidates. A diagnosis of liquid or solid masses is easily achieved, and thoracentesis is performed with a low risk of complications. Pulmonary lesions abutting the lung surface, and the anterior and superior mediastinum, which affect adults with malignant disease, are accessible. Prior US examination may guide the approach via VATS or thoracotomy. Vessels of the chest and of consolidations may be visualized without the use of contrast medium. US may be diagnostic in patients with suspected PEs with low-probability perfusion scanning. It may also guide the selection of more invasive imaging. The biopsy of solid lesions under continuous US guidance offers the highest diagnostic yield. US contributes to the bedside diagnosis of respiratory disorders in the ICU and provides rapid information in cases of pneumothorax, hemothorax, pleural or pericardial effusion, pneumonia and PE. US technology is constantly developing new modes for improved resolution and contrast. Future developments will undoubtedly advance our ability to visualize structures and tissue in a way that might not be imaginable today.
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Footnotes
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Abbreviations: PE = pulmonary embolism; US = ultrasound; VATS = video-assisted thoracoscopy
This work was supported by the Division of Pulmonary Medicine, Center of Internal Medicine, Nuremberg, Germany.
Received for publication April 16, 2001.
Accepted for publication March 5, 2002.
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