Ultrasound of the lung

Abstract

The CME review is intended to explain and discuss the clinical value of lung ultrasound but also to enable a pragmatically oriented approach by analyzing the clinical aspect. This includes knowledge of the pre-test probability, the acuteness of the disease, the current clinical situation, detection and/or characterization, initial diagnosis or follow up assessment and the peculiarities of exclusion diagnosis. Diseases of the pleura and lungs are described using these criteria with their direct and indirect sonographic signs and the specific clinical significance of ultrasound findings. The importance and criteria of conventional B-mode, color Doppler ultrasound with or without spectral analysis of the Doppler signal and contrast-enhanced ultrasound are discussed as well.

Key words

pleural effusion - pneumonia - guideline - lung embolism

Introduction

Traditionally, thoracic ultrasound is divided into different components: the thoracic wall, the diaphragm, the mediastinum, the lung parenchyma, and the pleura. Echocardiography is usually dealt with separately. In the CME article presented here (as one of three review articles), we aim to explain to interested readers what information can be gained from a lung parenchyma ultrasound and provide a pragmatic approach to analyzing the overall appearance. This involves knowledge of pre-test probability, the acuteness of the disease, the patient’s current clinical situation, and the diagnostic task: to detect or to characterize, to provide an initial diagnosis or a follow-up assessment, as well as the particular features of diagnosis by detection or exclusion. The setting for the diagnostic examination (outpatient, pre-admission, inpatient, emergency admission, ICU or pulmonary ward, clinic versus home visit) should also be taken into account. For information on the special features of thoracic ultrasound in children (pediatrics) [1] [2] [3] and in the elderly (geriatrics) [4], as well as artifacts [5], please refer to these recently published studies and position papers.

We outline the significance of conventional brightness-coded B-mode scans, color Doppler ultrasound (CDU), with or without spectral analysis of the Doppler signal, and contrast-enhanced ultrasound (CEUS), and the criteria for their use [6] [7] [8] [9] [10] [11] [12] [13]. We also briefly cover elastography [14] and ultrasound-guided interventions.

Peripheral Lung Consolidations

Diseases that feature peripheral pleural lung consolidations include acute and chronic diseases. The acute diseases of particular note are inflammatory diseases of the interstitium and alveolar spaces as an expression of viral and bacterial pneumonia, as well as vascular causes of pulmonary embolism. The chronic diseases include on the one hand primary and secondary neoplasia, with or without mechanical atelectasis, and on the other hand chronic inflammatory processes. When evaluating peripheral lung consolidations, the first thing to consider is the degree of acuteness (acute disease course) and the severity of the symptoms is critical. In indications that are not immediately urgent, the main focus is on differentiating between malignant and benign disease. In children, congenital lung consolidations such as pulmonary sequestrations [1] [2] are of particular significance.

Ultrasound Signs

In addition to its size and shape, e. g., with an acute or blunt angle, the consolidation is also assessed in terms of its margin and how well defined this is, its echo pattern (homogenous, non-homogenous), and vascular architecture showing either extension or destruction of the vessels in the surrounding area (assessment of neovascularization).

Notes 1

Neovascularization can only be detected using spectral analysis of the Doppler signal and CEUS.

Doppler ultrasound (visualization of vascularization) and CEUS are used for this (visualization of perfusion). The surrounding structures are also assessed e. g., pleural effusion, atelectasis, obstructive pneumonia, concomitant pneumonia, the multilocularity and respiratory displacement of the consolidation/mass, and diaphragmatic mobility. CEUS can be used to distinguish perfusion patterns of lung consolidations based on the:

1. Time to peak enhancement (arrival time) of contrast medium. Explanation: In young, healthy patients, the flow path of the pulmonary arteries become contrast-enhanced just a few (3–6) seconds after cubital injection of the contrast agent, whereas it takes 10–12 seconds for bronchoarterial contrast enhancement to begin.

2. Extent of enhancement,

3. Homogeneity of enhancement, and

4. Decrease of enhancement (wash out).

Pulmonary Embolism

Patients are examined for pulmonary embolism, or pulmonary infarction if they have the relevant constellation of risk factors; embolism and infarction occur more frequently than clinically expected. Contrast-enhanced computed tomography (CT angiography, CTA) is the method of choice for assessing hemodynamically relevant pulmonary embolisms. In patients with otherwise healthy lungs, perfusion scintigraphy has a similarly high diagnostic reliability as CT in detecting pulmonary embolisms; however, its usefulness is somewhat limited [15] in patients with comorbidities (such as pulmonary emphysema), and as a rule it is not available in acute situations.

Chest x-rays serve solely to exclude differential diagnoses for pulmonary embolism. While ultrasound as a complementary method is secondary to CTA, it has high informational value in its own right in settings in which CT is either not available or cannot be performed due to special circumstances (such pregnancy or hypersensitivity to the contrast agent). Ultrasound reveals subpleural consolidations with either no vascularization or reconstituted vascularization and with an absent or reduced air alveologram or air bronchogram, depending on the disease stage. In the case of pulmonary embolism, the lung consolidations are typically relatively small and round or triangular. In such cases, the use of color Doppler ultrasound is essential. Contrast-enhanced ultrasound is also helpful for difficult differential diagnoses as it confirms the infarction due to the absence of contrast or a non-homogenous area of contrast [16] [17] ([Fig. 1]).

Fig. 1 a Pulmonary embolism. Multiple peripheral lung consolidations (more than 10), examined in B-mode scan with high-resolution linear ultrasound probe (a, b, c) and in contrast enhanced mode with a convex transducer (d, e). The lung consolidations show minimal or no contrast enhancement.

Often it is possible to see a centrally occluded vessel at the base of a triangular marker consolidation. Besides evidence of the consolidation, ultrasound also enables concomitant assessment of the heart for right ventricular strain and examination of the leg veins for diagnosis of thrombosis as important sources of embolism (this is called the triple diagnostic). The aim is to look for direct evidence of thrombi, right atrial dilation (compared with left atrial dilation), right ventricular dilation with wall motion abnormalities in the presence of preserved apical contractility (McConnell’s sign), paradoxical septal motion, and tricuspid regurgitation (with flow speeds > 250 cm/s) and with elevated pulmonary artery pressure (> 40 mmHg).

Pneumonia

Pneumonia is characterized by acute symptomatology (fever and dyspnea), demonstrable infiltrate, and possibly by complications that can be detected by ultrasound (metapneumonic effusion, empyema, abscess). The sonomorphology of pneumonia is determined by its different etiologies (e. g., bacterial or viral), and the pattern of involvement (e. g., alveolar, interstitial), as well as the stage of the disease [18] [19] [20] [21].

Bacterial Pneumonia

Various forms of manifestation are differentiated: extensive bilobar, lobar, segmental, but also less obvious predominantly interstitial forms. Bronchopneumonic infiltrates (BPI) can occur in a wide range of patterns which often do not extend to the periphery of the lung. BPI without direct pleural contact are not visible on ultrasound; however, their presence may be suspected based on indirect signs (secondary effusion, comet-tail artifacts). The ultrasound signs of pneumonia depend on the stage of the disease and on the displacement of air by inflammatory fluids (exudate). In addition to the localization and size criteria mentioned above, the ultrasound signs include a moderately homogenous echo pattern (similar to that of the liver), accompanied by alveolar (air alveologram) or bronchial (air bronchogram) air pockets, depending on the disease stage with or without fluid (fluid bronchogram) in the small airways; this tends to occur distally to areas of stenosis. According to its extent and localization, the margin may be sharp or ill-defined, as well as regularly (or smoothly) delimited or irregular (depending on the congestion or reconstitution). In the absence of air or fluid pockets, segmental and lobar infiltrates can bear a striking resemblance to liver parenchyma (hepatization); this makes it possible to visualize the vascular tree of the pulmonary arteries and veins. Color Doppler ultrasound shows vessels in a regular arrangement with significant diastolic blood flow, in contrast to the scenario with pulmonary embolism (vessel occlusion at the base). The usefulness of ultrasound in assessing pneumonia decreases in the late stages of the disease due to re-aeration with shadowing air echoes (“crepitatio redux”). As a concomitant phenomenon, comet-tail artifacts may be detected at the margins of the infiltrates, pleural effusions, and enlarged mediastinal lymph nodes. Differentiating between the initial pneumonic infiltrate and other subpleural lung consolidations depends on the patient’s acute clinical symptoms, as well as the size and vascularization and perfusion characteristics of the consolidation (Doppler ultrasound, CEUS).

Complications

Complications of pneumonia include necrosis (more frequent) and abscess formation (less frequent, < 6 %), pleural empyema, and acute respiratory distress syndrome (ARDS) (common description: white lung) ([Fig. 2]).

Fig. 2 a Pneumonia with metapneumonic effusion (a) and abscess formation (b).

Necrosis and Abscesses

Necrosis and abscesses within pulmonary infiltrates can appear as less echogenic, more or less sharply defined areas of differing sizes. If there is bronchial involvement, air pocket, or the air-fluid level can be visualized by ultrasound. The visualization of necrosis and abscesses is significantly improved by the use of contrast enhanced ultrasound. While abscesses up to 20 mm in size are initially treated conservatively, from 20–30 mm ultrasound-guided aspiration is used for diagnostic and therapeutic purposes, and with even larger abscesses without bronchial involvement, percutaneous abscess drainage may be indicated.

Special Features

Pneumonia associated with infarction may show peripheral areas with no contrast enhancement on CEUS. Pneumonia-associated pulmonary infarction, for example in COVID infections, is characterized on CEUS by pleural areas with an absence of perfusion [7] [11]. Chronic pneumonia with delayed regression can present complex echogenicity with disturbed perfusion; in such cases, neoplastic consolidation must be ruled out histologically.

Special features of tuberculosis are exudative pleural effusion, marked mediastinal lymphadenopathy, polymorphism of subpleural consolidations, air reflection with air-filled cavities, as well as fragmentation of the visceral pleura. On CEUS, tubercular infiltrates are characterized by delayed bronchoarterial perfusion. It is important to watch out for extrapulmonary manifestations. The overall picture may help to point suspicion towards tuberculosis [23].

Viral Pneumonia

Ultrasound signs of viral interstitial pneumonia have long been classified as of little diagnostic value [5] [24] [25] [26] ([Fig. 3]), but have acquired great diagnostic importance in the context of the COVID pandemic. Depending on the stage, increased B-line artifacts may initially be detected in COVID pneumonia as a reflection of interstitial inflammation and fluid retention. Later, multiple small (< 20 mm) multilocular subpleural consolidations can be seen on both sides, with or without air echoes, and with irregularity/fragmentation of the pleural line. Due to the necessary hygienic measures, the use of handheld ultrasound devices in COVID has become established at some centers [27] [28]. Although in the context of a high clinical pretest probability for COVID, this is a spot diagnosis, these ultrasound phenomena are nevertheless not specific but can also be observed in other interstitial pneumonias [29].

Fig. 3 a Viral pneumonia, in this case COVID infection. B-line artifacts (“curtain”, a) and multilocular small (< 20 mm) subpleural consolidations (b). For comparison, the representation in the CT (c).

Typically, all viral pneumonias show an absence of relevant pleural effusion. However, high-resolution ultrasound probes are almost always able to detect small quantities of pleural fluid in the posterior and lateral costodiaphragmatic recess, especially with patients in the sitting position [2] [11] [19] [20] [22] [24] [29] [30] [31] [32].

Fungal Pneumonia

In the field of hematology, fungal pneumonia is a significant issue in immunosuppressed patients. PLUS can detect aspergilloma in pleural pneumonic consolidations due to a lack of contrast uptake in CEUS. 

Parasitic Pneumonia

Parasite-related consolidations include peripherally located echinococcosis, which is also characterized in the lungs by polycystic consolidation with lack of enhancement of the walls in CEUS [33] ([Fig. 4]).

Fig. 4 Echinococcosis as a partially cystic-appearing peripheral lung consolidation.

Autoimmune Pneumonia

This includes organizing forms of pneumonia; these are classed among the chronic forms of pneumonia and can only be distinguished from neoplasms through histological analysis ([Fig. 5]).

Fig. 5 a Wegener’s granulomatosis. CEUS is helpful in assessing blood flow. In contrast to pulmonary embolism, marked contrast enhancement is found.

Atelectasis

Atelectasis is defined as the collapse of parts of the lung, characterized by reduced aeration in the lung parenchyma. A distinction is made between compression atelectasis, resorption atelectasis, and obstructive atelectasis, each of which has different causative pathologies (e. g., pleural effusion in compression and tumor in obstruction). For purposes of differential diagnosis, it is helpful to observe the correlation between the extent of the effusion and the size of the atelectasis: if there is minimal effusion with a large area of atelectasis, this should always arouse suspicion of infiltrative or obstructive components. CEUS can be used to delineate the central mass underlying obstructive atelectasis. In contrast to this expansive pneumonic infiltrate with a convex margin, compression atelectasis usually exhibits a concave margin and shows regular vessels running in a straight line on CDU. Spectral analysis of the Doppler signal and CEUS allow pulmonary arterial vessels to be identified in atelectasis[34] [35] ([Fig. 6]).

Fig. 6 Atelectasis with concave margins in contrast to expansive pneumonic infiltrate. Atelectasis is characterized by very early contrast enhancement of the pulmonary arteries, prior to enhancement of the bronchial arteries and systemic circulation.

Notes 2

In general, atelectasis has concave margins, in contrast to pneumonic infiltrate which has convex margins.

Notes 3

With atelectasis there is very early contrast uptake in the pulmonary arteries before the bronchial arteries and systemic circulation.

Neoplastic Lung Parenchymal Changes

Neoplastic lung parenchymal changes are divided into primary tumors (e. g., lung carcinoma) and secondary tumors (metastasis). Concomitant changes in the surrounding lung parenchyma tend to be less common in metastases than in primary tumors. If the mass is in a peripheral location, ultrasound is a valuable aid to differential diagnosis. Important aspects to mention here are assessment of the tumor dignity, clarification of differential diagnoses, and potentially ultrasound-guided puncture, if this is indicated considering the patient’s age, comorbidities, and wishes, as well as the recommendation of the interdisciplinary tumor board. Ultrasound evidence of infiltration of the parietal pleura or thoracic wall, as a descriptor of T3 disease, has special clinical significance due to its influence on therapeutic strategies. Direct evidence of tumor expansion into the thoracic wall and/or destruction of ribs are considered to be definite signs of infiltration. Widening of the parietal pleura and restricted mobility of the lesions with pulmonary location in relation to the thoracic wall during breathing are considered to be uncertain signs. As peritumoral inflammatory responses can also lead to adhesion of the pleural layers, neither of the last two signs are considered to be evidence of infiltration. When investigating neoplastic changes it is also important to assess their surroundings, especially in order to detect vascular complications (such as tumor infiltration of the vena cava or heart, thrombosis, or upper inflow congestion), pleural metastases, and cervical and mediastinal lymph node metastases. Evidence of cervical and clavicular lymph node metastases, including, if required, confirmation through ultrasound-guided cytology and histology, is proof of N3-stage disease; this means a curative therapeutic approach is no longer possible. Distant metastasis can also be detected on ultrasound, or demonstrated by ultrasound-guided biopsy/aspiration. This applies, for example, for liver and adrenal metastases, infradiaphragmatic lymph node metastases, nodular pleural thickening, and malignant pleural or pericardial effusions. Lung carcinomas grow in a displacing and/or destructive manner, usually tend to be oval-shaped, and often show marked peripheral vascularization with neoangiogenesis of pathological vessels at the tumor margin. Local blood vessels are displaced or infiltrated. After pretest probability (malignant disease known or probable), contrast enhanced-ultrasound is the most useful in determining the dignity of peripheral lung consolidations as it enables determination of the time to peak, analysis of perfusion (present or absent), and characterization of the vascularity. Contrast-enhanced ultrasound enables at least rough differentiation based on the time to enhancement relative to that of the pulmonary arteries and systemic circulation (bronchial arteries). Depending on underlying comorbidities, contrast enhancement in the pulmonary arteries occurs just a few (3–6) seconds after injection, while enhancement in the bronchial arteries via systemic circulation occurs after approximately 12 ± 2 seconds, simultaneously with enhancement of the thoracic wall, liver or spleen as reference organs. Since tumor neoangiogenesis develops predominantly from the bronchial arteries, this type of perfusion is preferentially observed in neoplastic processes ([Fig. 7], [8]). CEUS has great clinical value in differentiating between vital and necrotic tumor tissue, as well as tumor tissue and atelectasis; it should be performed prior to every ultrasound-guided tumor biopsy in order to avoid the risk of a false negative result [36] [37] [38]. Color Doppler ultrasonography with spectral analysis also often makes it possible to differentiate between inflammatory (with pulmonary arterial supply) and neoplastic (with predominantly bronchial arterial supply) circumscribed changes. The higher the resistive index (RI), the greater the likelihood of a malignant etiology. Similar to other organ systems, the RI threshold value can be specified as approximately 0.8 [39]. In terms of differential diagnoses, inflammatory causes (e. g., granulomatosis, carnifying pneumonia) must be considered, as well as scars and necrosis [40] [41] [42].

Fig. 7 a Neoplastic lung parenchymal changes in B-mode scan (a) and CEUS (b–e). A typical feature is contrast enhancement occurring from the periphery towards the center. Note that lung parenchyma with pulmonary artery perfusion shows earlier contrast enhancement than a lung tumor, which is supplied by the bronchial arteries

Fig. 8 a Neoplastic lung parenchymal changes, lipoma (a). A typical feature is the very limited contrast enhancement (b, arrow pointing to an individual arterial blood vessel).

Contusion, Hemorrhage

Lung contusions with hemorrhage are observed following rib fractures, for example. They can range from slight to very large, with or without pleural effusion. CEUS allows reliable delineation of vascularized subpleural consolidations, as the bleeding does not take up the contrast medium. Intraparenchymal lung hemorrhages in atelectactic lung tissue can also be visualized with CEUS [43] ([Fig. 9]).

Fig. 9 Contusion, peripheral hemorrhage after fall. Contrast-enhanced ultrasound shows no contrast uptake in the hemorrhage.

Conflict of Interest

Declaration of financial interests

Receipt of research funding: Yes, from another institution (pharmaceutical or medical technology company, etc.); receipt of payment/financial advantage for providing services as a lecturer: no; paid consultant/internal trainer/salaried employee: no; patent/business interest/shares (author/partner, spouse, children) in company: no; patent/business interest/shares (author/partner, spouse, children) in sponsor of this CME article or in company whose interests are affected by the CME article: no.

Declaration of non-financial interests

The authors declare that there is no conflict of interest.

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Publication History

Article published online:
13 April 2023