Ultraschall Med 2023; 44(01): 14-35
DOI: 10.1055/a-1885-5664
Continuing Medical Education

Pulmonary Sonography – Neonatal Diagnosis Part 1

Article in several languages: English | deutsch
Clinic for Pediatrics and Adolescent Medicine, Sana Kliniken Duisburg GmbH, Duisburg, Germany
› Author Affiliations
 

Abstract

Diseases of the respiratory system are among the main problems of premature patients in the neonatal intensive care unit. Radiography of the thorax is the gold standard of imaging. This results in high cumulative radiation exposure with potential negative long-term consequences. Ultrasound examination of thoracic structures represents a promising radiation-free and ubiquitously available alternative.

A healthy, ventilated lung can only be imaged via artifacts, since total reflection of the sound waves occurs due to the high impedance difference between tissue and air-filled lung. Pathologies of pleura and subpleural lung tissue lead to changes in the acoustic properties of the tissue and thus to variations in the artifacts that can be imaged. The main sonographic characteristics of pulmonary pathology are: pleural line abnormalities, increased B-lines and comet-tail artifacts, lung consolidations, a visible pulmonary pulse, pleural sliding abnormalities, and visualization of effusions. Deviations from normal sonographic findings can be assigned to specific underlying pathophysiologies, so that conclusions about the disease can be drawn in conjunction with the clinical symptoms.


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Introduction

Pulmonary disease due to lung immaturity, disorders of postnatal adaptation and ventilator-associated pulmonary complications are common causes of neonatal morbidity and mortality. Radiography of the thorax in the AP beam is still usually considered the gold standard of imaging. This leads to repeated radiation exposure of immature patients in the neonatal ICU with potential negative long-term consequences. Lung ultrasound is an alternative, radiation-free procedure for the diagnosis and monitoring of pleural and pulmonary diseases. Sonography is rapidly available bedside almost anywhere at any time. Therefore, lung ultrasound is an ideal point-of-care procedure to answer clinical questions directly at the patient’s bedside. The aim should therefore be to familiarize as many physicians as possible working in this field with the methodology and its possibilities and limitations. This work intends to convey the basics of lung ultrasound, taking into account the special features of premature and newborn babies.

Learning Goals
  • Understanding the basics of device settings and examination flow

  • Acquisition of normal lung ultrasound findings

  • Recognition of pathological lung ultrasound findings

  • Determining the possible causes of pathological findings

  • Understanding the limitations of lung ultrasound


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Device settings and examination sequence

In the neonatal stage, lung ultrasound employs almost exclusively high-resolution linear or hockey stick transducers (7–20 MHz). These enable a high level of detail resolution and achieve – with the small body volume and thinness of the neonatal chest wall – for almost all questions a sufficient depth of penetration. A penetration depth of 3–5 cm should be selected as a basic setting, adapted to the body weight, with focusing at the level of the pleural line. The overall gain should be adjusted so that strongly echogenic structures are not over-illuminated and better contrast can be achieved. The transducer is placed perpendicular to the thoracic wall and the lung surface is fanned as completely as possible in the longitudinal and transverse or intercostal oblique directions on both sides from ventral, lateral and dorsal. The lungs can be divided into different areas for more accurate assessment and description of findings. The posterior and anterior axillary lines serve to distinguish into one ventral, lateral and dorsal lung field for each hemithorax. A further subdivision of these quadrants can be made in the transverse direction centrally into upper and lower fields ([Fig. 1]) [1] [2] [3] [4] [5]. Depending on the position of the ribs and the region this result in 3–5 intercostal spaces per that an assessment of the area. The supine position is optimal for ventral examination, and the prone position is optimal for dorsal examination. For critically ill patients, repositioning may be ruled out and instead the patient may be turned slightly to one side alternately to allow visualization of as much of the lung surface as possible. Another important sectional plane is the upward sloping upper abdominal cross-section, which allows assessment of the dorsobasal lung fields from ventrally and a view of the diaphragmatic recesses.

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Fig. 1 Schematic representation of the lung regions. In the longitudinal direction, each half of the thorax is differentiated into an anterior, lateral, and posterior lung field. The sternal line (SL), anterior axillary line (VAL), posterior axillary line (HAL), and vertebral line (VL) serve as anatomical landmarks. A further subdivision into upper and lower field can be made by central separation in transverse direction. In preterm infants, bisection of the lateral areas is often omitted because of the small surface area.

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Normal Findings in B-Mode

The structures of the thoracic wall, including the ribs, are displayed close to the transducer. A dorsal acoustic shadow is created behind bony structures. Adjacent to this is the pleural line, a delicate hyperechogenic line corresponding to the tissue-air boundary ([Fig. 2], [Video 1]) [6]. Due to the large difference in impedance between the tissue of the thoracic wall and the air-filled lung, total reflection and axial mirroring of the sound waves occurs at the tissue-air interface ([Fig. 2], [Video 1]). When the sound waves strike the mirror surface, they are completely reflected and sent back to the transducer. A small portion of the sound waves is absorbed by the transducer and processed by the ultrasound device; the remainder is reflected again at the transducer surface. This process continues until the sound energy is consumed. The longer the signal travels back and forth between the transducer and the mirror surface until it is processed, the deeper the ultrasound device positions the suspected structure in the image. This is how the repetition echoes, which decrease in intensity towards the bottom, are created ([Fig. 2], [Video 1]) [7]. In lung ultrasound, these horizontal reverberation artifacts are referred to as A-lines ([Fig. 2]). In the moving image, one can also see the pleural sliding, an atemosynchronous displacement of the pleural line with respect to the structures of the thoracic wall ([Video 1]) [8] [9]. It is essential to note that only ultrasound artifacts can be imaged below the tissue-air interface. Central processes which are surrounded by air-filled lungs are not accessible to sonography. In addition, the sound waves are absorbed in the area of bony structures, so that an assessment of the lungs behind them is also not possible. The lung surface can be sonographically detected in approximately 70 % of fully ossified thoracic structures [2] [5] [6]. In premature and newborn infants, however, the sonic window is larger because the still cartilaginous rib-sternum region allows almost complete coverage of the ventral lung surface ([Fig. 2a]). Because the air-filled lung can only be visualized via artefacts the sonographically generated image is more dependent on the selected transducer, the device settings and the experience of the examiner than in the presentation of other organs. Device functions for image optimization, such as harmonic imaging, compound imaging or crossbeam technique, suppress ultrasound artifacts and thus significantly influence the display of signals relevant for lung ultrasound [1] [3].

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Fig. 2 Normal findings. a Parasternal longitudinal section from ventral view. The structures of the thoracic wall (double arrow), including the ribs (open arrow heads), are displayed close to the transducer. Due to their high sound conduction velocity, the still cartilaginous, hypoechoic ribs lead to an axial misplacement of the adjacent pleural line, which means that it is not displayed as a straight line, but as a wavy line. Below the hyperechogenic pleural line, only artifacts are imaged due to total reflection and specular reflection. Horizontal repetition echoes of decreasing intensity, the A-lines (arrowheads), appear. In addition, reflections of the rib cartilage can be seen (oblique arrows). b Longitudinal section dorsal view. In contrast to the ventral view, the bony ribs (open arrow heads) lead to an absorption of the sound waves with a dorsal sound shadow. c M-mode showing the seashore or sandy beach sign with regular pleural sliding. The structures of the thoracic wall appear as smooth, parallel lines ⇒ waves (double arrow). The adjacent prominent hyperechogenic line corresponds to the pleural line. Due to pleural sliding, the subsequent repetition echoes are slightly blurred ⇒ beach. In addition, the lung pulse (asterisk) can be identified.

Video 1 Regular pleural sliding in a paravertebral longitudinal section. Respiratory synchronous displacement of the hyperechogenic pleural line against the structures of the thoracic wall.


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Normal Findings in M-Mode

With M-mode, pleural sliding can be visualized in an image and thus documented ([Fig. 2c]). Although the structures of the thoracic wall move little during quiet breathing and thus smooth horizontal lines are imaged in M-mode, due to pleural sliding fine- to coarse-grained imaging of the repeat echoes occurs below the pleural line. The so-called seashore or sandy beach sign is visible ([Fig. 2c]). Under good examination conditions, the lung pulse can also be imaged in M-mode as additional information ([Fig. 2c]). This involves the conduction of pulsations from the heart and great vessels to the lungs, which results in a small vibration of the pleural line and a vertical artifact in the region of the dorsally-located reverberation artifacts ([Fig. 2c]). This change is synchronous with the QRS complex and does not involve thoracic wall structures [6] [9]. If the seashore sign and lung pulse cannot be identified optimally, an adjustment of the run in M-mode should be made. Slowing the transducer movement may facilitate visualization of pleural sliding, and increasing the speed may facilitate identification of the pulmonary pulse.


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Pathological Findings

The healthy, air-filled lung can only be visualized via its artifacts. Pathological changes in the pleura and subpleural lung tissue alter the acoustic properties of the tissue, leading to typical visualizable changes in the ultrasound artifacts. As long as the lungs are filled with air, only artifacts can be imaged sonographically, and central lung areas cannot be detected [6] [10].

Increased vertical reverberation artifacts and lung consolidations are the main sonographic characteristics of pulmonary disease. In addition, pathology may be manifested by pleural line abnormalities or a visible pulmonary pulse. Pathological processes in the pleural space are presented by pathological pleural sliding or the appearance of effusions.

B-Lines and Interstitial Syndrome

B lines are hyperechoic, vertical repeat echoes originating perpendicularly from the pleural line, which extend laser-like from the pleural line to the end of the screen area and move synchronously with pleural sliding ([Fig. 3]) [9] [11]. B-line diagnostics are primarily dependent on the transducer and device settings selected, which is why most authors recommend disabling device options for image optimization for B-line imaging [1] [3] [12]. According to current knowledge, the classic B-lines, which originate from an intact, smooth pleural line, arise at air-fluid interfaces in the pleural interstitium and the pleural alveoli. Detection of single B-lines, especially in the basal lung fields, is considered physiological. Evidence of more than 2 B-lines per intercostal space in the longitudinal section in each region examined is considered an interstitial syndrome ([Fig. 3]). Interstitial syndrome is a sign of increased fluid content in the lungs. B-line diagnostics should thus enable a semi-quantitative assessment of the air-to-fluid ratio. Increasing fluid content and decreasing air content of the pleural lung tissue results in an increased visualization of B-lines with a simultaneous decrease in the visualization of A-lines ([Fig. 3]). B-lines may occur singly or confluent in one or more intercostal spaces. The maximum variant is referred to as a sonographically white lung ([Fig. 3]) [2] [6] [9] [10]. Increased vertical repeat echoes are seen in interstitial and alveolar-interstitial pulmonary edema caused by inflammatory or non-inflammatory processes as well as in lung parenchymal diseases. In fibrotic parenchymal disease, vertical reverberation artifacts are most likely caused by scarred interstitial changes with increase in density of the interstitium. Vertical repeat echoes emanating from an irregular and fragmented pleural line are referred to by some authors as comet-tail artifacts in contrast to classic B-lines. They are considered as an indication of inflammatory or fibrotic processes ([Fig. 4a]) [5]. However, most scientific work in the field of neonatology currently does not yet differentiate between classic B-lines and comet tail artifacts [9] [10] [13].

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Fig. 3 B-lines and interstitial syndrome in parasternal longitudinal section. Vertical repetitive echoes originating from the pleural line show the B-lines (asterisks), which extend like a laser beam from the pleural line to the end of the screen area. B-lines may occur singly or merge in single or multiple intercostal spaces (brackets). As the intensity of the B-lines increases (left to right), fewer and fewer A-lines (arrowheads) can be seen. If only confluent B-lines without displayable A-lines can be imaged, this is referred to as a sonographically white lung (far right image).
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Fig. 4 Comet-tail artifacts. a Longitudinal ventral section in a premature infant at 23 + 3 gestational weeks with bronchopulmonary dysplasia (2 months old, FiO2 0.75 under invasive ventilation). The pleural line presents irregularly and distinctly fragmented, and is interrupted by several smaller and larger hypoechogenic structures (reduced ventilation). Vertical repeat echoes emanate from the edges of these hypoechogenic areas, which are referred to as comet tail artifacts (asterisks). A-lines (arrowheads) can only be imaged in isolated cases. b Intercostal cross-section of reduced ventilation near the pleura in a 26-gestational week preterm infant with respiratory failure due to a severe postnatal CMV infection (6 weeks old, FiO2 0.8 under invasive ventilation). Vertical repeat echoes, resembling B-lines, emanate from the irregular, deep margins of homogeneous, low-echo consolidations (microatelectases/dystelectases) with fine echo texture. The comet-tail artifacts merge and can only be differentiated to a limited extent.

In premature and newborn babies, an increased interstitial fluid content can be caused by physiological processes in the context of postnatal adaptation as well as by pathological processes. Because the lung physiologically has an increased fluid content in the premature and neonatal stage, the above definition cannot be used synonymously to differentiate between physiological and pathological findings. In most healthy, mature newborns the pulmonary adaptation process is completed within the first 24 hours of life [13] [14]. In contrast, B-lines and interstitial syndrome persist much longer in preterm infants, and norm definitions adapted to gestational week and postnatal age are lacking. However, a ubiquitous white lung is considered pathologic at any age.


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Consolidation

Lung consolidation refers to a non-ventilated or poorly ventilated area of the lung, which can thus be visualized using ultrasound. In this case, the air in the alveoli may be displaced or replaced by fluid or ventilation of the alveoli may be inadequate due to insufficient ventilation, airway obstruction or alveolar collapse [2] [9]. Consequently, consolidations are seen in all diseases with inflammatory, mechanically or thromboembolically reduced ventilation. Even minimal subpleural decreased ventilation can be detected with ultrasound. Similarly, reduced ventilation of entire lobes of the lung can be visualized ([Fig. 5]); however, only consolidations in contact with the lung surface can be detected [2] [6]. Consolidations lead to an interruption of the pleural line and appear hypoechoic in B-mode ([Fig. 4], [5]). In larger consolidations, the lung tissue resembles liver or spleen in echogenicity and echotexture ([Fig. 5]). A-lines can no longer be seen below consolidations. The deep, irregular margins of the consolidations are origins of hyperechoic, vertical repeat echoes resembling B-lines ([Fig. 4], [5]). In contrast, they do not arise in the area of the pleural line and are therefore classified as comet-tail artifacts ([Fig. 4b]) [2] [3]. The contained residual air appears as tubular or tree-like hyperechogenic structure in the bronchial system (aerobronchogram) or as islands of residually ventilated alveoli ([Fig. 4b], [5]). In contrast to a static aerobronchogram, movements of the residual air in the bronchial system can be observed during inspiration and expiration in a dynamic aerobronchogram. A dynamic aerobronchogram argues against complete mechanical obstruction of the bronchial system ([Video 2]).

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Fig. 5 Consolidations. a Dorsal cross-section in a preterm infant 23 + 3 gestational weeks on day 3 of life (FiO2 0.60 under invasive ventilation). A coarse- to fine-grained altered pleural line is seen at the left edge of the image. This pathology extends beyond the subpleural region and corresponds to poorly ventilated lung tissue. This poorly ventilated area with a large amount of displayable residual air merges into a more extensive reduced ventilation on the right edge of the picture with residual air that is hardly displayable. In this area, the lung tissue appears liver-like. b Dorsal cross-section of a 26-gestational week preterm infant with respiratory failure due to a severe postnatal CMV infection (6 weeks old, FiO2 0.65 under invasive HFO ventilation). A coarsely fragmented, partially absent pleural line is evident. The consolidated lung tissue appears hypoechogenic with hyperechogenic, bulbous air inclusions and irregular deep margins. A-lines can no longer be displayed dorsal to the consolidation. c Dorsal cross-section in a twin premature infant at 23 + 4 gestational weeks at 4 weeks of age (FiO2 0.85 under invasive HFO ventilation). The pleural line cannot be displayed in large sections. In these areas, the visceral pleura appears as a very faint hyperechoic line (arrow). A small amount of fluid in the pleural space can also be used to delineate the parietal pleura (arrowheads). In the remaining sections, the pleural line is roughly fragmented. The consolidated lung tissue, which extends into deep regions of the lung, appears hypoechogenic with fine echotexture, few roundish to tubular hyperechogenic air remnants, and irregularly configured deep margins. d Upper lobe atelectasis in a neonate with vein of Galen malformation on invasive ventilation (FiO2 0.40). Extensive under-ventilation (atelectasis) of the right upper lobe in cross-section. Lung tissue resembles the spleen. Hyperechogenic residual air is barely visible. Since the entire cross-section of the upper lobe is affected, the edges of the reduced ventilation correspond to the pleura, which is why this consolidation is bordered by smooth edges on all sides.

Video 2 Dynamic aerobronchogram. Dorsal cross-section in the left lower quadrant in a twin premature infant at 23 + 1 weeks of gestation with respiratory global insufficiency (2nd day of life, FiO2 0.80 under invasive ventilation). There is a large, hypoechoic consolidation with a lot of residual air. Multiple, hyperechoic air reflexes move synchronously with breathing in the fluid-filled, hypoechoic bronchi.


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In the case of persistently detectable, cystically altered intrathoracic solid tissue or abnormal echogenicity and echotexture, congenital malformations or tumors must also be considered in the differential diagnosis. In such cases, cross-sectional imaging methods can contribute to further etiological clarification [5] [7].


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Changes to the Pleural Line

The pleural line is a delicate, hyperechoic line that moves synchronously with breathing ([Video 1]). It does not correspond to the direct visualization of the pleura but rather to the tissue-air boundary. If there is some free fluid in the pleural space, it is possible to differentiate the pleural space and the parietal pleura from the tissue-air boundary using high-resolution linear transducers ([Fig. 5c]). The visceral pleura can only be imaged directly as a very delicate hyperechoic line if there is a lack of air in the lung tissue close to the pleura ([Fig. 5c]) [1] [6] [9]. Pleural and subpleural pathologies result in abnormal presentation of the pleural line. The pleural line can be thickened (> 0.5 mm), irregular, fragmented, coarse-grained or fine-grained, or absent ([Fig. 5]). The comet-tail artifacts described above originate from small sonographically mostly hypoechoic changes near the pleura ([Fig. 4], [5]). Pleural pathologies can indicate both insufficient ventilation of the lung tissue near the pleura and inflammatory or fibrotic changes [1] [13] [14] [15] [16]. Accurate assessment of pleural and subpleural changes is best achieved with high-resolution linear transducers at low penetration depth and focusing on the level of the pathologies using the device options for image optimization.


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Visible Lung Pulse

The lung pulse corresponds to the transmission of pulsations from the heart and large vessels to the lung tissue. Under physiological conditions, the lung pulse can only be displayed using M-mode ([Fig. 1c]). If the physical properties of the lung increasingly correspond to those of a solid organ, e. g. in the case of massive alveolo-interstitial fluid accumulation or pronounced insufficient ventilation, the lung pulse is visible in the moving image ([Video 3]) [9]. However, the significance of a visible lung pulse in very small premature babies is controversially discussed due to the special anatomical conditions.

Video 3 Visible lung pulse. Ventral longitudinal section in a preterm triplet at 33 + 6 weeks of gestation with grade III respiratory distress syndrome at the age of 3 hours. Confluent vertical reverberation artifacts are predominant, producing the image of a white lung. In addition, a thickened, coarsely modified pleural line, small subpleural consolidations, and the pulmonary pulse visible on the B-scan can be seen.


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Abnormalities of Pleural Sliding

Absent pleural sliding is when the respiratory-synchronous displacement of the lungs against the structures of the thoracic wall cannot be visualized in the moving image. Absence of pleural sliding is the main sonographic criterion for pneumothorax ([Video 4]) [17]. However, abnormalities of pleural sliding are not unique to pneumothorax. Regular pleural sliding cannot be demonstrated even with missing or reduced lung ventilation due to tube malposition in the esophagus, selective endobronchial intubation ([Video 5]), extensive atelectasis ([Video 6]) or massive hyperinflation. After pleurodesis or in the presence of pleural adhesions of other causes, assessment of pleural sliding can no longer be used for pneumothorax diagnosis [1] [9] [16] [18]. The sonographic characteristics of pneumothorax are presented in the second part of this paper.

Video 4 Absence of pleural sliding in pneumothorax. Right-sided pneumothorax in a premature baby at 23 + 6 SSW under invasive ventilation. No pleural sliding can be visualized in the moving image. The movements below the tissue-air boundary correspond to reflections of the movements of the thoracic wall structures. In addition, the reflections of the rib cartilages can be seen very clearly.


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Video 5 Absence of pleural sliding during therapeutic selective endobronchial intubation on the left side for bullous emphysema on the right side. On the right side, no regular pleural sliding can be visualized in the parasternal longitudinal section. In addition, consolidations can be seen with the onset of atelectasis. In the case of bullous emphysema, sections with horizontal repeat echoes (overinflated, bullous areas) appear despite the lack of ventilation – the development of complete atelectasis on the right side lasted more than 12 hours. The minimal respiratory movements are due to declining relaxation with little self-breathing.


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Video 6 Abnormalities of pleural sliding in extensive atelectasis. Dorsal longitudinal section in a premature baby at 23 + 1 weeks of gestation at the age of 6 weeks with global respiratory failure in the context of bronchopulmonary dysplasia (FiO2 0.90 under invasive ventilation). Dorsocranially, hardly any movement of the lung against the structures of the thoracic wall can be seen, but further caudally, pleural sliding is clearly detectable.


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Effusion

Ultrasound allows detection of even a few milliliters of intrapleural fluid in premature and newborn infants when used correctly [1] [19] [20]. Depending on the position, pleural effusion collects at the deepest point of the pleural cavity, which is why the supine position is preferable to rule out a pleural effusion. The most important sections are the subxiphoid upper abdominal section, which is inclined upwards, and the sternal and lateral longitudinal sections showing the diaphragmatic recess. Using ultrasound, the extent of the effusion can be identified and monitored serially without radiation at the patientʼs bedside. A pronounced basal compression atelectasis can be an indication of a relevant amount of effusion ([Fig. 6]). Ultrasound alone can neither clarify the etiology of an effusion with sufficient certainty nor replace a diagnostic puncture – but it enables an optimal assessment of the internal structure of the effusion and is thus process far superior to MRI and CT. However, when assessing the echogenicity and echotexture of an effusion, it must always be taken into account that a purely serous effusion usually appears anechoic, but on the other hand an anechoic effusion is not evidence of transudate. Inflammatory, chylous or bloody pleural effusions usually present sonographically as complex effusions with fine or coarse internal reflexes, but can also appear anechoic depending on the transducer used and the time of the examination ([Fig. 6], [7]). However, detection of a complex effusion excludes a transudate with a high degree of probability and should therefore be substantially supplemented by a diagnostic puncture for precise etiological clarification. This can be performed safely with ultrasound guidance even with the smallest amounts of effusion [1] [5] [19] [20]. The correct position of a chest drain cannot usually be confirmed with sufficient sensitivity by sonography alone. However, in cases of doubt, ultrasound is superior to AP radiography when depicting whether the drainage of the lung is ventral or dorsal ([Fig. 8]).

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Fig. 6 Effusion. a + b Bilateral serous effusion in the subxiphoid transverse section of the upper abdomen, which is inclined upwards a and transverse flank section b in a preterm infant with sepsis. The effusion presents anechoic. Compression of the lung results in consolidation of the basal lung fields, allowing the lung to be delineated in a crescent shape with smooth borders within the effusion. c+d Right-sided chylous effusion. An effusion with coarse, inhomogeneous internal reflexes can be visualized cranially of the liver in the upward sloping upper abdominal cross-section c. Under therapy, the effusion – shown here in a longitudinal section at the level of the midaxillary line – is predominantly free of echoes with individual septa d.
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Fig. 7 Hemothorax in a neonate. a An upwardly inclined cross-section of the upper abdomen shows a complex effusion cranial to the left lobe of the liver in the region of the left hemithorax. Overlying the consolidated lung ventrally is a solid-appearing, inhomogeneous process with liver-like echogenicity and echotexture, surrounded by an effusion with fine internal reflexes (erythrocytes). The consolidated, sickle-shaped lung (arrows) is difficult to differentiate from the inhomogeneous effusion. b Image of the left diaphragmatic recess in flank section. The proportionally aerated basal lung (arrow) presents hyperechogenic with dorsal vertical repeat echoes. The lung has an inhomogeneous mass (blood coagulum) surrounded by an effusion with fine internal reflexes (erythrocytes). The parietal pleura can be distinguished from the structures of the thoracic wall and the diaphragm as a delicate, hyperechoic line.
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Fig. 8 Ultrasound image of a chest drain in a dorsal intercostal cross-section in a preterm infant with refractory chylothorax. In longitudinal section, the walls of the chest drain appear as hyperechogenic parallel double contours enclosing an anechoic lumen. The left image shows the passage into the pleural cavity. By moving the transducer, the drainage can be followed further intrathoracically (right image). In addition, a thickened pleura and multiple subpleural consolidations are evident. The pleura transitions paravertebrally into a pleural rind (asterisk), which causes displacement and compression of the lung.

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Conclusions

For a long time, the air-filled lung was considered to be an organ inaccessible to sonography. In the meantime, many studies have shown that ultrasound artifacts of the lungs do allow for a sonographic assessment. A sound knowledge of age-related normal findings as well as typical pathologic findings and their significance is a necessary prerequisite for the correct interpretation of lung sonographic findings. Sonographic hallmarks of respiratory disease include: Pleural line changes, increased B-lines and comet-tail artifacts, lung consolidations, pleural sliding abnormalities, a visible lung pulse, and visualization of effusions. These deviations from normal sonographic findings are caused by changes in the acoustic properties of the pleura and subpleural lung tissue and can be attributed to specific underlying pathophysiologies. Together with the clinical picture, conclusions can be drawn about the existing disease.

However, the examiner should always be aware that mostly artifacts are displayed, that different pathologies can therefore produce very similar or even identical sonographic images and that the display is also influenced by the selected transducer and the device settings. Lung ultrasound findings can therefore always only be interpreted correctly in conjunction with the patientʼs clinical symptoms. Pulmonary sonography is a very sensitive imaging modality for near-surface lung pathologies, but central pathologies surrounded by air-filled lung are not amenable to ultrasound examination. Assessment can therefore only be limited to the lung surface actually examined, which is why a comprehensive examination is desirable for a reliable diagnosis.


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Conflict of Interest

Declaration of financial interests

Receipt of research funding: no; 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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Correspondence

Dr. Simone Schwarz
Clinic for Pediatrics and Adolescent Medicine, Sana Kliniken Duisburg GmbH
Zu den Rehwiesen 9–11
47055 Duisburg
Germany   
Phone: ++49/2 03/7 33 32 96   

Publication History

Article published online:
08 September 2022

© 2022. Thieme. All rights reserved.

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  • References

  • 1 Jaworska J, Buda N, Ciuca IM. et al. Ultrasound of the pleura in children, WFUMB review paper. Med Ultrason 2021; 23 (03) 339-347
  • 2 Dietrich CF, Buda N, Ciuca IM. et al. Lung ultrasound in children, WFUMB review paper (part 2). Med Ultrason 2021; 23 (04) 443-452
  • 3 Mathis G, Horn R, Morf S. et al. WFUMB position paper on reverberation artefacts in lung ultrasound: B-lines or comet-tails?. Med Ultrason 2021; 18 (01) 70-73
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Fig. 1 Schematic representation of the lung regions. In the longitudinal direction, each half of the thorax is differentiated into an anterior, lateral, and posterior lung field. The sternal line (SL), anterior axillary line (VAL), posterior axillary line (HAL), and vertebral line (VL) serve as anatomical landmarks. A further subdivision into upper and lower field can be made by central separation in transverse direction. In preterm infants, bisection of the lateral areas is often omitted because of the small surface area.
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Fig. 2 Normal findings. a Parasternal longitudinal section from ventral view. The structures of the thoracic wall (double arrow), including the ribs (open arrow heads), are displayed close to the transducer. Due to their high sound conduction velocity, the still cartilaginous, hypoechoic ribs lead to an axial misplacement of the adjacent pleural line, which means that it is not displayed as a straight line, but as a wavy line. Below the hyperechogenic pleural line, only artifacts are imaged due to total reflection and specular reflection. Horizontal repetition echoes of decreasing intensity, the A-lines (arrowheads), appear. In addition, reflections of the rib cartilage can be seen (oblique arrows). b Longitudinal section dorsal view. In contrast to the ventral view, the bony ribs (open arrow heads) lead to an absorption of the sound waves with a dorsal sound shadow. c M-mode showing the seashore or sandy beach sign with regular pleural sliding. The structures of the thoracic wall appear as smooth, parallel lines ⇒ waves (double arrow). The adjacent prominent hyperechogenic line corresponds to the pleural line. Due to pleural sliding, the subsequent repetition echoes are slightly blurred ⇒ beach. In addition, the lung pulse (asterisk) can be identified.
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Fig. 3 B-lines and interstitial syndrome in parasternal longitudinal section. Vertical repetitive echoes originating from the pleural line show the B-lines (asterisks), which extend like a laser beam from the pleural line to the end of the screen area. B-lines may occur singly or merge in single or multiple intercostal spaces (brackets). As the intensity of the B-lines increases (left to right), fewer and fewer A-lines (arrowheads) can be seen. If only confluent B-lines without displayable A-lines can be imaged, this is referred to as a sonographically white lung (far right image).
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Fig. 4 Comet-tail artifacts. a Longitudinal ventral section in a premature infant at 23 + 3 gestational weeks with bronchopulmonary dysplasia (2 months old, FiO2 0.75 under invasive ventilation). The pleural line presents irregularly and distinctly fragmented, and is interrupted by several smaller and larger hypoechogenic structures (reduced ventilation). Vertical repeat echoes emanate from the edges of these hypoechogenic areas, which are referred to as comet tail artifacts (asterisks). A-lines (arrowheads) can only be imaged in isolated cases. b Intercostal cross-section of reduced ventilation near the pleura in a 26-gestational week preterm infant with respiratory failure due to a severe postnatal CMV infection (6 weeks old, FiO2 0.8 under invasive ventilation). Vertical repeat echoes, resembling B-lines, emanate from the irregular, deep margins of homogeneous, low-echo consolidations (microatelectases/dystelectases) with fine echo texture. The comet-tail artifacts merge and can only be differentiated to a limited extent.
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Fig. 5 Consolidations. a Dorsal cross-section in a preterm infant 23 + 3 gestational weeks on day 3 of life (FiO2 0.60 under invasive ventilation). A coarse- to fine-grained altered pleural line is seen at the left edge of the image. This pathology extends beyond the subpleural region and corresponds to poorly ventilated lung tissue. This poorly ventilated area with a large amount of displayable residual air merges into a more extensive reduced ventilation on the right edge of the picture with residual air that is hardly displayable. In this area, the lung tissue appears liver-like. b Dorsal cross-section of a 26-gestational week preterm infant with respiratory failure due to a severe postnatal CMV infection (6 weeks old, FiO2 0.65 under invasive HFO ventilation). A coarsely fragmented, partially absent pleural line is evident. The consolidated lung tissue appears hypoechogenic with hyperechogenic, bulbous air inclusions and irregular deep margins. A-lines can no longer be displayed dorsal to the consolidation. c Dorsal cross-section in a twin premature infant at 23 + 4 gestational weeks at 4 weeks of age (FiO2 0.85 under invasive HFO ventilation). The pleural line cannot be displayed in large sections. In these areas, the visceral pleura appears as a very faint hyperechoic line (arrow). A small amount of fluid in the pleural space can also be used to delineate the parietal pleura (arrowheads). In the remaining sections, the pleural line is roughly fragmented. The consolidated lung tissue, which extends into deep regions of the lung, appears hypoechogenic with fine echotexture, few roundish to tubular hyperechogenic air remnants, and irregularly configured deep margins. d Upper lobe atelectasis in a neonate with vein of Galen malformation on invasive ventilation (FiO2 0.40). Extensive under-ventilation (atelectasis) of the right upper lobe in cross-section. Lung tissue resembles the spleen. Hyperechogenic residual air is barely visible. Since the entire cross-section of the upper lobe is affected, the edges of the reduced ventilation correspond to the pleura, which is why this consolidation is bordered by smooth edges on all sides.
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Fig. 6 Effusion. a + b Bilateral serous effusion in the subxiphoid transverse section of the upper abdomen, which is inclined upwards a and transverse flank section b in a preterm infant with sepsis. The effusion presents anechoic. Compression of the lung results in consolidation of the basal lung fields, allowing the lung to be delineated in a crescent shape with smooth borders within the effusion. c+d Right-sided chylous effusion. An effusion with coarse, inhomogeneous internal reflexes can be visualized cranially of the liver in the upward sloping upper abdominal cross-section c. Under therapy, the effusion – shown here in a longitudinal section at the level of the midaxillary line – is predominantly free of echoes with individual septa d.
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Fig. 7 Hemothorax in a neonate. a An upwardly inclined cross-section of the upper abdomen shows a complex effusion cranial to the left lobe of the liver in the region of the left hemithorax. Overlying the consolidated lung ventrally is a solid-appearing, inhomogeneous process with liver-like echogenicity and echotexture, surrounded by an effusion with fine internal reflexes (erythrocytes). The consolidated, sickle-shaped lung (arrows) is difficult to differentiate from the inhomogeneous effusion. b Image of the left diaphragmatic recess in flank section. The proportionally aerated basal lung (arrow) presents hyperechogenic with dorsal vertical repeat echoes. The lung has an inhomogeneous mass (blood coagulum) surrounded by an effusion with fine internal reflexes (erythrocytes). The parietal pleura can be distinguished from the structures of the thoracic wall and the diaphragm as a delicate, hyperechoic line.
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Fig. 8 Ultrasound image of a chest drain in a dorsal intercostal cross-section in a preterm infant with refractory chylothorax. In longitudinal section, the walls of the chest drain appear as hyperechogenic parallel double contours enclosing an anechoic lumen. The left image shows the passage into the pleural cavity. By moving the transducer, the drainage can be followed further intrathoracically (right image). In addition, a thickened pleura and multiple subpleural consolidations are evident. The pleura transitions paravertebrally into a pleural rind (asterisk), which causes displacement and compression of the lung.
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Abb. 1 Schematische Darstellung der Lungenareale. In Längsrichtung erfolgt je Thoraxhälfte die Differenzierung in ein vorderes, seitliches und hinteres Lungenfeld. Als anatomische Landmarken dienen die Sternal-Linie (SL), die vordere Axillarlinie (VAL), die hintere Axillarlinie (HAL) und die Vertebrallinie (VL). Eine weitere Unterteilung in Ober- und Unterfeld kann durch mittige Trennung in Querrichtung erfolgen. Bei Frühgeborenen wird aufgrund der geringen Oberfläche häufig auf die Zweiteilung der lateralen Areale verzichtet.
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Abb. 2 Normalbefund. a Parasternaler Longitudinalschnitt von ventral. Schallkopfnah zeigen sich die Strukturen der Thoraxwand (Doppelpfeil) inklusive der Rippen (offene Pfeilköpfe). Die noch knorpeligen, echoarmen Rippen führen durch ihre hohe Schall-Leitungs-Geschwindigkeit zu einer axialen Fehlplatzierung der angrenzenden Pleuralinie, wodurch diese nicht als gerade Linie, sondern gewellt abgebildet wird. Unterhalb der hyperechogenen Pleuralinie werden durch Totalreflexion und Spiegelung nur Artefakte abgebildet. Es zeigen sich horizontale, in ihrer Intensität abnehmende Wiederholungsechos, die sog. A-Linien (Pfeilköpfe). Zudem kann man angedeutet Spiegelungen der Rippenknorpel erkennen (schräge Pfeile). b Longitudinalschnitt von dorsal. Im Unterschied zur Darstellung von ventral führen die knöchernen Rippen (offene Pfeilköpfe) zu einer Absorption der Schallwellen mit dorsalem Schallschatten. c M-Mode mit Darstellung des Seashore- oder Sandy-Beach-Sign bei regelrechtem Pleuragleiten. Die Strukturen der Thoraxwand stellen sich als glatte, parallele Linien dar ⇒ Wellen (Doppelpfeil). Die angrenzende prominente hyperechogene Linie entspricht der Pleuralinie. Durch das Pleuragleiten bilden sich die folgenden Wiederholungsechos leicht verschwommen ab ⇒ Strand. Zudem kann der Lungenpuls (Sternchen) identifiziert werden.
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Abb. 3 B-Linien und interstitielles Syndrom im parasternalen Longitudinalschnitt. Es zeigen sich von der Pleuralinie ausgehende vertikale Wiederholungsechos, die sog. B-Linien (Sternchen), welche sich wie ein Laserstrahl von der Pleuralinie bis zum Ende der Bildschirmfläche erstrecken. B-Linien können einzeln auftreten oder in einem oder mehreren Interkostalräumen miteinander verschmelzen (Klammern). Mit von links nach rechts zunehmender Intensität der B-Linien lassen sich immer weniger A-Linien (Pfeilköpfe) darstellen. Lassen sich nur noch konfluierende B-Linien ohne darstellbare A-Linien abbilden, bezeichnet man dies als sonografisch weiße Lunge (Bild rechts außen).
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Abb. 4 Kometenschweif-Artefakte. a Longitudinalschnitt von ventral bei einem Frühgeborenen von 23 + 3 SSW mit Bronchopulmonaler Dysplasie (2 Monate alt, FiO2 0.75 unter invasiver Beatmung). Die Pleuralinie stellt sich unregelmäßig und deutlich fragmentiert dar. Sie wird durch mehrere kleinere und größere hypoechogene Strukturen (Minderbelüftungen) unterbrochen. Von den Rändern dieser hypoechogenen Areale gehen vertikale Wiederholungsechos aus, welche als Kometenschweif-Artefakte (Sternchen) bezeichnet werden. A-Linien (Pfeilköpfe) können nur vereinzelt abgebildet werden. b Pleuranahe Minderbelüftung im interkostalen Querschnitt bei einem Frühgeborenen der 26. SSW mit respiratorischer Insuffizienz im Rahmen einer schweren postnatalen CMV-Infektion (6 Wochen alt, FiO2 0.8 unter invasiver Beatmung). Von den irregulären, tiefen Rändern der homogen, echoarmen Konsolidierungen (Mikro-Atelektasen/Dystelektasen) mit feiner Echotextur gehen vertikale Wiederholungsechos aus, welche B-Linien ähneln. Die Kometenschweif-Artefakte konfluieren und sind nur noch eingeschränkt zu differenzieren.
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Abb. 5 Konsolidierungen. a Dorsaler Querschnitt bei einem Frühgeborenen von 23 + 3 SSW am 3. Lebenstag (FiO2 0.60 unter invasiver Beatmung). Am linken Bildrand zeigt sich eine grob- bis feinkörnig veränderte Pleuralinie. Diese Pathologie erstreckt sich bis über die subpleurale Region hinaus und entspricht minderbelüftetem Lungengewebe. Dieses minderbelüftete Areal mit viel darstellbarer Restluft geht in eine ausgedehntere Minderbelüftung am rechten Bildrand mit kaum darstellbarer Restluft über. In diesem Bereich stellt sich das Lungengewebe Leber-ähnlich dar. b Dorsaler Querschnitt bei einem Frühgeborenen der 26. SSW mit respiratorischer Insuffizienz im Rahmen einer schweren postnatalen CMV-Infektion (6 Wochen alt, FiO2 0.65 unter invasiver HFO-Beatmung). Es zeigt sich eine grobfragmentierte, teils fehlende Pleuralinie. Das konsolidierte Lungengewebe zeigt sich hypoechogen. Das konsolidierte Lungengewebe zeigt sich hypoechogen mit hyperechogenen, scholligen Lufteinschlüssen und unregelmäßigen tiefen Rändern. Dorsal der Konsolidierung lassen sich keine A-Linien mehr darstellen. c Dorsaler Querschnitt bei einem Zwillingsfrühgeborenen von 23 + 4 SSW im Alter von 4 Wochen (FiO2 0.85 unter invasiver HFO-Beatmung). Die Pleuralinie lässt sich in großen Abschnitten nicht darstellen. In diesen Bereichen bildet sich die Pleura visceralis als sehr zarte hyperechogene Linie ab (Pfeil). Durch etwas Flüssigkeit im Pleuraspalt ist auch eine Abgrenzung der Pleura parietalis (Pfeilköpfe) möglich. In den übrigen Abschnitten stellt sich die Pleuralinie grob fragmentiert dar. Das konsolidierte Lungengewebe, welches sich bis in tiefe Regionen der Lunge erstreckt, zeigt sich hypoechogen mit feiner Echotextur, wenigen rundlichen bis tubulären hyperechogenen Luftresten und irregulär konfigurierten tiefen Rändern. d Oberlappenatelektase bei einem Neugeborenen mit Vena Galeni Malformation unter invasiver Beatmung (FiO2 0.40). Ausgedehnte Minderbelüftung (Atelektase) des rechten Oberlappens im Querschnitt. Das Lungengewebe ähnelt dem der Milz. Es lässt sich kaum hyperechogene Rest-Luft darstellen. Da der ganze Querschnitt des Oberlappens betroffen ist, entsprechen die Ränder der Minderbelüftung der Pleura, weshalb diese Konsolidierung allseits von glatten Rändern begrenzt wird.
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Abb. 6 Ergüsse. a + b Beidseitiger seröser Erguss im nach oben geneigten subxiphoidalen Oberbauchquerschnitt a und transversalen Flankenschnitt b bei einem Frühgeborenen im Rahmen einer Sepsis. Der Erguss stellt sich echofrei dar. Durch Kompression der Lunge kommt es zur Konsolidierung der basalen Lungenfelder, wodurch sich die Lunge sichelförmig mit glatter Begrenzung innerhalb des Ergusses abgrenzen lässt. c + d Rechtsseitiger chylöser Erguss. Im nach oben geneigten Oberbauchquerschnitt lässt sich kranial der Leber ein Erguss mit groben, inhomogenen Binnenreflexen darstellen c. Unter Therapie zeigt sich der Erguss – hier in einem Longitudinalschnitt auf Höhe der mittleren Axillarlinie dargestellt – überwiegend echofrei mit einzelnen Septen d.
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Abb. 7 Hämatothorax bei einem Neugeborenen. a Im nach oben geneigten Oberbauchquerschnitt zeigt sich kranial des linken Leberlappens im Bereich des linken Hemithorax ein komplexer Erguss. Der konsolidierten Lunge liegt ventral ein solide wirkender, inhomogener Prozess mit Leber-ähnlicher Echogenität und Echotextur auf, umgeben von einem Erguss mit feinen Binnenreflexen (Erythrozyten). Die konsolidierte, sichelförmige Lunge (Pfeile) lässt sich nur schwer von dem inhomogenen Erguss abgrenzen. b Darstellung des linken Recessus diaphragmaticus im Flankenschnitt. Die anteilig belüftete basale Lunge (Pfeil) stellt sich hyperechogen mit dorsalen vertikalen Wiederholungsechos dar. Der Lunge liegt eine inhomogene Masse (Blutkoagel) an, umgeben von einem Erguss mit feinen Binnenreflexen (Erythrozyten). Die Pleura parietalis lässt sich als zarte, hyperechogene Linie von den Strukturen der Thoraxwand sowie von denen des Zwerchfells abgrenzen.
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Abb. 8 Sonografische Darstellung einer Thoraxdrainage in einem dorsalen interkostalen Querschnitt bei einem Frühgeborenen mit therapierefraktärem Chylothorax. Die Wände der Thoraxdrainage stellen sich im Längsschnitt als hyperechogene parallele Doppelkonturen dar, welche ein echofreies Lumen einschließen. Im linken Bild ist der Durchtritt in die Pleurahöhle dargestellt. Durch Verschiebung des Schallkopfes lässt sich die Drainage weiter nach intrathorakal verfolgen (rechtes Bild). Zudem sind eine verdickte Pleura sowie multiple subpleurale Konsolidierungen zu erkennen. Die Pleura geht paravertebral in eine Pleuraschwarte (Sternchen) über, welche eine Verlagerung und Kompression der Lunge verursacht.