Introduction

Chest plain films still form the mainstay of paediatric chest imaging in most routine queries. However, there are instances where radiographs reveal equivocal information or are unable to define a diagnosis; furthermore, some conditions necessitate frequent follow-up investigations that may add up to a significant radiation burden, particularly considerable in infants and children with their increased radiation sensitivity.

Ultrasound (US) of the paediatric chest has become an established imaging tool that may supplement plain film findings helping to reduce other ionizing (sectional) imaging in a variety of paediatric conditions [1–12]. US has been shown to offer valuable imaging alternatives, both enabling diagnosis and additional information in equivocal findings on radiographs or even replacing follow-up examinations (for example in pleural effusions or diaphragmatic palsy).

This review briefly outlines the technical requisites for chest US applications and its diagnostic potential. It furthermore will discuss US restrictions, mention some rare applications, and discuss the potential role of chest US in imaging algorithms of certain conditions. Echocardiography, mediastinal, as well as (endoscopic) intra-operative chest US will not be included.

Equipment and requirements

Requirements depend on patient age, site of the pathology and sonographic access. For chest wall assessment as well as for US of the superficial pleural and lung space a high resolution linear transducer is recommended. Frequencies vary from 5 to 15 MHz. For intercostal access to deeper spaces a sector or vector array transducer proves helpful; again frequencies vary with age and depth of the focused pathology. For transabdominal access-using the liver, the fluid-filled stomach, or the spleen as a sonographic window to the diaphragm and basal chest spaces-sector and curved linear array transducers are helpful. A relatively high frame rate, harmonic imaging, and a crisp post-processing may also be helpful. Colour-Doppler sonography (CDS) is used for assessment of abscesses, space-occupying lesions, vascular pathology and sequestration. M-Mode may be helpful for assessment and documentation of diaphragmatic movement.

Additional to these technical requirements, the profound knowledge of potential paediatric and neonatal chest disease and its differential diagnosis is mandatory. In general US can be considered a supplement to plain film and should not be seen as the one and only primary imaging tool for chest queries; however, in many conditions the combination of US and plain film will reveal a definite diagnosis and most of the treatment-relevant information.

Diseases suitable for chest ultrasound

The following lists the most important paediatric chest US applications, including a description of typical features and discussion of the role of US in diagnostic imaging algorithms. Note that US is excellent for assessment of the thymus and thus is the first choice for assessment of a radiographically unclear widened mediastinum.

Pleural effusion

US is very sensitive in detecting particularly latero-dorsal and basal pleural effusions, even more sensitive than plain film for small amounts of fluid, and thus can be used for diagnosis and follow-up [1–7, 13–17]. US helps to differentiate locculated and/or echogenic (“complicated”) from clear and unseptated (“uncomplicated“) collections, and US is even more sensitive than CT for depicting septations within an effusion. These abilities may in conjunction with clinical information impact management (e.g., only follow-up without puncture in minimal uncomplicated reactive effusion, single drainage of an unseptated collection, or pigtail catheter placement in large complicated and potentially loculated empyema-very much also depening on local variations in treatment plans). Or US may reveal valuable information for deciding between various alternative treatment options (e.g., thoracoscopic intervention, open surgery, or image guided percutaneous drainage-potentially with additional instillation of fibrinolytic agents for breaking down of septae allowing a successful conservative treatment) (Fig. 1) [10, 11, 15–19]. However, note that US does not always allow for definite specification of the disease or differentiation of transudation versus exudate, haemorrhagic versus proteinous, reactive versus inflammatory, or cardiogenic versus chylous effusions.

Fig. 1
figure 1

Ultrasound appearance and findings in pleural effusions. (a) US, sagital section, trans-abdominal acquisition, right side: infant with clear pleural fluid above the diaphragm, with central air-filled lung (= echogenic structure) in an uncomplicated/simple pleural effusion. (b) US, axial section, trans-abdominal acquisition, slightly tiled cranially, same patient as Fig. 1a: note the clear pleural fluid on the right side, whereas the pleural collection on the lift side contains some particles with dorso-basal sedimentation and a debris-fluid level (haemorrhagic), indicating a complicated pleural effusion

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Particularly for follow-up, a standardised patient and transducer position is recommended to allow for comparability of measurement (e.g., sitting, as thus the fluid collects in the lower thorax). Due to the complex geometry of effusions an accurate assessment of its volume is difficult. Particularly in large collections a transhepatic or transabdominal access may prove helpful, as well as extended field-of-view techniques. Finally, US offers a safe and reliable real-time guidance for interventions [2–7, 10, 11, 20–22]. It may help to define the best location for incision and drainage, allows for real-time control during the puncture and catheter placement, and offers post-interventional follow-up (Fig. 2).

Fig. 2
figure 2

US-guided puncture and drainage of pleural effusions. Slightly rotated axial section, trans-abdominal acquisition, tiled cranially for needle visualisation during puncture. US clearly demonstrates the very echogenic, air-filled needle during a diagnostic and therapeutic puncture of a pleural fluid collection

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Pulmonary processes

As soon as the air-filled lung or the air in the lung is replaced by fluid, consolidation, or by another non-aerated process, these areas become accessible to US, provided the process reaches the chest wall or the diaphragm. Thus US may help to differentiate various radiographically unspecific findings by revealing more information about the structure of the process, e.g., liquid or solid, with maintained lung anatomy or destruction, with or without perfusion alterations, etc. [1–13, 23–26]. Thus, US may help to avoid additional imaging. However, as soon as suspicion of a tumour arises, or US is unable to properly answer all treatment-relevant questions (e.g., preoperatively, only partial visualisation of the process, information on other lung areas essential, etc.), additional imaging by contrast-enhanced CT or MRI becomes mandatory.

Atelectasis

Atelectasis can be seen on US, as this process usually reaches the pleura. It may be due to compression or obstruction. US signs for atelectasis are no visible air or bronchi in the liver-like parenchyma (“hepatisation”) and a triangular shape with convex or straight margins. However, some residual undulating aeration may be observed during respiration in some cases, or bronchi may be filled with fluid (“fluid-bronchogram”) then only distinguishable from vessels by CDS. Note that US cannot reliably differentiate an atelectasis from (hypostatic or broncho-) pneumonia, and often dystelectasis is associated with severe pneumonia. (Peripheral) pulmonal infarctions are rare in the paediatric setting, though sometimes discovered unexpectedly; in these conditions CDS may help establishing the diagnosis applying the same diagnostic criteria as in adults [25].

Infectious conditions

The typical US image of pneumonia is a liver-like appearance of the parenchyma, often with some residual air in central echogenic bronchi that are accompanied by the vascular bundle creating linear echogenicities (= “air-bronchogram”) (Fig. 3) [26]. One may find flow in the pulmonary vessels; using duplex-Doppler sonography trace analysis a differentiation of pulmonary artery brunches, pulmonary veins and bronchial arteries becomes feasible, helping to differntiate pneumonia from infarction or necrosis (Fig. 4a). Complications within inflammatory processes lead to disruption of the lung anatomy as well as regional perfusion defects; these criteria help to sonographically demonstrate abscess formation (Fig. 4b). Once an abscess is located, US may offer a safe guide for puncture and drainage. Particularly when US matches clinical findings US and chest film may suffice for diagnosis, and cross-sectional imaging may be avoided.

Fig. 3
figure 3

Ultrasound appearance and findings in lung consolidations or atelectasis. (a) US, axial-transverse section, lateral inter-costal access, left side: atelectatic lung adjacent to an uncomplicated pleural effusion. Note that dystelectasis cannot reliably be differentiated sonographically from (broncho-)pneumonia or hypostatic pneumonia, and sometimes these occure combined. (b) US, axial-transverse section, lateral inter-costal access, lower lobe right side: liver like appearance of a segmental pneumonia, with some simple secondary pleural effusion. (c) US, tilted transverse section, ventro-lateral inter-costal access, upper lobe right side: abscess formation is visualised by depicting hypoechoic confluent cyst-like areas within the pneumonic lung

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Fig. 4
figure 4

Colour Doppler sonography in pneumonia and its complications. (a) US, transverse section, ventro-lateral inter-costal access, right side: colour Doppler sonography depicts pulmonary vessels in this pneumonia, enabling focussed duplex tracing for flow analysis in the pulmonary arteries-in this case helping to rule out embolic pulmonary infarction. (b) US, transverse section, ventro-lateral inter-costal access, upper lobe right side, same patient as Fig. 3c: power Doppler (= amplitude coded colour Doppler sonography) demonstrates the highly vascularised pneumonic lung, with lack of visible perfusion in the necrotic abscess centre, thus clearly demonstrating the abscess formation

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Congenital pulmonal malformations

With the advances in foetal sonography many thoracic foregut malformations are detected prenatally. They all need postnatal assessment, confirmation and follow-up, particularly as we only start learning about the natural course of some of these conditions. As many of these may regress spontaneously early imaging is helpful. Ultrasound can be used for imaging all lesions that are solid and/or liquid and reach the chest wall or the diaphragm. The major findings with more or less typical US features are:

  • sequestrations usually are echogenic and homogenous masses with sharp borders; often CDS can identify a large vessel (Fig. 5) [1–4, 8, 11, 27–35]. The feeding artery usually arises from the aorta and should be identified by meticulous scanning, whereas the draining vein either may drain to the systemic or to the pulmonary circulation-this is more difficult to differentiate on sonography; sometimes the shape of the duplex trace can help differentiate the two venous systems. Note that (extra-lobar) sequestration can be found that are also juxta- or even infra-diaphragmatic. Sometimes cysts may be present, then indicating a hybrid lesions (of CCAM and sequestration).

  • Congenital cystic adenomatoid malformation (CCAM) can be macro-cystic, micro-cystic, or a mixture of medium size cysts with solid aspects; the respective histology defines the US appearance (Fig. 6) [2–4, 8, 11, 36–39].

  • Bronchial cysts are only visible on US as long as they are fluid filled; if they have a connection with the bronchial tree, they may exhibit fluid air levels [37–39]. When the fluid is absorbed, an air-filled cyst remains, then becoming inaccessible by US.

Fig. 5
figure 5

US in sequester. (a) Chest plain film with a homogeneous mass in the left lower thorax projecting over the heart silhouette. (b) Colour Doppler sonography depicts a pair of vessels in this echogenic, triangular-shaped basal lesion of the left basal thorax, consistent with a sequester with a large artery feeding arising from the abdominal aorta

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Fig. 6
figure 6

US in neonatal CCAM. (a) Chest film with a small, hardly visible consolidation in the lower right lung, projecting over the liver (=>). (b) A parasagital longitudinal high resolution US from a baso-dorsal approach demonstrates a small congenital cystic adenomatoid malformation of the right lung (+1 +1). Note the complex structure of partially macrocystic (+2 +2) lesion

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Cysts, tumours/neoplasms, and other thoracic masses

Thoracic masses are usually depicted by plain film; US may help to differentiate the nature of the mass. Though cystic chest lesions and potential tumours may be assessed sonographically, differentiation of the various entities cannot regularly be achieved. Only indirect signs may hint towards the diagnosis, such as:

  • a clear cyst, particularly in a neonate or infant, will probably represent a bronchial, pleural, or pericardial cyst or a CCAM [2–4, 8, 11, 36–39]. In older children other entities that may be more difficult to differentiate by US such as hydatide disease or (postinfectious/posttraumatic) encapsulated effusions must be considered [40].

  • A cyst with irregular walls and nodular soft tissue components may hint towards pulmoblastoma or teratoma, particularly if calcifications are present. (Fig. 7).

  • a soft tissue mass with regional compression and small punctuate calcifications may indicate a neuroblastoma.

  • An echogenic mass in a neonate or infant with a (large) artery deriving from the systemic circulation will represent a sequestration [1–4, 8, 11, 27–35].

  • Central cysts with multi-layered walls that resemble bowel wall may indicate oesophageal duplications or diaphragmatic hernia.

Fig. 7
figure 7

US, other paediatric thoracic space occupying lesions. A large complex mass in the right hemithorax that was found to be a partially cystic, partially necrotic and haemorrhagic pulmoblastoma

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However, as soon as the suspicion of a tumour arises, if US is unable to properly answer all relevant questions, or for differential diagnosis additional imaging by contrast-enhanced CT or MRI will be mandatory for further assessment, staging, and surgery planning. However, in children thoracic tumours or (particularly pleural) metastasis are rare, and therefore US of these masses is less important than in adults. If visible sonographically US may offer image guidance for biopsies.

Other typical paediatric chest masses are often mediastinal, such as lymphoma, oesophageal duplication, thoracic neuroblastoma, mediastinal teratoma, ventral meningocele, and thymus tumours-however, the discussion of these entities is beyond the scope of this review. The same applies to cardiac masses or pericardial effusions and cysts.

Diaphragmatic conditions

The most common query that can best be answered by US is diaphragmatic palsy or relaxation. Ultrasound as a real-time investigation can nicely visualise diaphragmatic movement during breathing, and US can compare both sides. Documentation is difficult if video-clips cannot be archived. Motion(m)-mode improves documentation of (disturbed) motion, and the m-mode trace allows a semi-quantitative assessment, not only for comparison of both sides, but also during follow-up [41–47] (Fig. 8).

Fig. 8
figure 8

Motion-mode US for assessment of diaphragmatic respiratory motion. (a) US, paramedian sagital acquisition through the fluid-filled stomach, left side: motion-mode track demonstrating diminished, varying, but regularly undulating respiratory diaphragmatic respiratory motion in spite of the an obvious pleural effusion. (b) US, sagital section, trans-abdominal acquisition, right side: m-mode track demonstrates complete lack of respiratory motion in a patient with a complex basal pleural collection (empyema); the diaphragmatic condition was assumed to be a possible cause for the severe complication of pleuro-pneumonia. (c) These 3 images of the same patient demonstrate the complimentary aspect of radiograph, B-mode US and m-mode. The chest film shows a reduced translucency of the left hemithorax with no significant mediastinal shift in an infant after recent cardiac surgery. The US (axial transabdominal view of the left hemithorax) demonstrates subtotal atelectasis with secondary basal hypostatic pneumonia (airbronchogram) and minimal pleural effusion. The m-mode track (axial section, trans-abdominal acquisition, slightly tiled cranially, left side) demonstrates reduced respiratory motion in postoperative partial diaphragmatic relaxation, thus influencing respiratory support management

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The echogenic structure cranial to the liver (and spleen) represents the air-filled lungs; the diaphragm itself can usually not be seen unless there is pleural fluid adjacent to the thoracic border of the diaphragm. Then the diaphragmatic muscle can be seen as a hypoechoic layer over the liver and the spleen. Diaphragmatic hernias can thus only be visualised if abdominal content herniated through the gap and displaces the lung, or with pleural effusions. US works perfectly for diagnosis of congenital diaphragmatic hernia on foetal US (no air in the lungs or bowel) and can be used in neonates as well, particularly if there is only little abdominal gas that interferes with sonographic access [2–4, 11, 48, 49] (Fig. 9). Small gaps without herniation of major structures, however, can be missed, such as diaphragmatic lacerations in a posttraumatic setting. Hiatus hernia or intrathoracic position of the stomach can only be seen when the stomach is filled with tea that allows manifestation of herniation (during filling) and delineation of these structures, provided sufficient sonographic access [50–52]. Thus, US may find and demonstrate such a hernia or even the rare intrathoracic kidney, but is unreliable in ruling out particularly small or intermittent diaphragmatic herniation.

Fig. 9
figure 9

US in diaphragmatic hernia. (a) A chest plain film suggests a bilateral diaphragmatic hernia. (b) US of the same patient (as in Fig. 6a) demonstrates the fluid-filled stomach reaching up into the left thoracic cavity through a large diaphragmatic defect, confirming the diagnosis; on the right side some parts of the liver were up, too (no image)

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Chest wall applications

Sometimes, visible or palpable chest wall complaints may lead to a focussed US investigation of the suspected area. Using high-frequency linear transducers the superficial structures are readily accessible to US. As soft tissues and non-ossified parts of the ribs are better seen sonographically than on radiographs (and often even CT), US represents the primary modality in imaging these conditions [2–4, 8, 53].

One condition in the neonate may be a swollen breast (Fig. 10a). Here US may help to delineate not only physiological changes during breast feeding caused by maternal hormones, such as (asymmetrically) prominent breast tissue or ectatic cyst-like ducts, but may also help to diagnose abscess formations, cysts or haematomas, the latter being more common in older girls after trauma. Furthermore, US is used in the assessment of other paediatric breast masses such as gynaecomastia [10, 11, 53–58].

Fig. 10
figure 10

US potential in chest wall conditions. (a) US in a neonate with a swollen painful breast reveals an abscess with regionally reactively enlarged lymph nodes (+ +). (b) Chest wall US-in this case using a vector array to allow for depth penetration and access intercostally-reveals the large complex tumour of the chest wall that extends quite deeply and consists of solid and cystic aspects; the cysts are filled with echoes, due to recent haemorrhage into this mixed, partially cystic lymphangioma

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Another typical clinical query is a chest wall lump, as clinically the differentiation between a deep haematoma, a lymph node, a tumourous lesion or a rib anomaly may be difficult. US enables depiction of rib variations, demonstrating the cartilaginous fused parts of ribs or cartilaginous exostoses [53]. It may also show periostal changes or subperiostal haematoma after injury sometimes even in radiographically occult fractures, particularly in the early posttraumatic setting. Ultrasound may demonstrate haemangiomas or cystic lymphangioma, often with intermittent haemorrhage into some compartments creating a conglomerate of mixed simple and complicated cysts (Fig. 10b). Only small vessels are incidentally visible within the septae on CDS. Although US accurately demonstrates lymphangiomas, additional imaging (MRI) may become indicated for visualisation of the entire extend, particularly if there is suspicion of deep or mediastinal involvement. Rare other chest wall tumours such as Askin tumour or osteosarcoma may be seen by US that demonstrates the destructive nature of the tumour and its relation to the partially destroyed rib; however, these conditions always require further (sectional) imaging, both for assessment of the local status as well as for staging.

Discussion

Ultrasound primarily is used for assessment of chest wall abnormalities and for further evaluation of equivocal radiographic findings, usually opacities. Typical scenarios are the opaque (hemi)thorax, pleural effusions, and focal chest opacities-provided they reach the chest wall or the diaphragm for sonographic access (Fig. 11). In some conditions US offers a reliable follow-up method, such as in pleural effusions or prenatally diagnosed foregut malformations. And US is an established portable imaging tool for “FAST” and effective assessment of trauma patients for potential pleural and pericardial collections during evaluation and stabilisation at the emergency room. Finally US can be used as an image guidance for various interventional procedures, mostly punctures and drainages of fluid collections or abscesses, but also (less frequent) for guiding biopsies. With this considerable potential of paediatric chest US and particularly if mediastinal pathologies are additionally included in the definition “paediatric chest ultrasound”, US today should play a major role in paediatric chest imaging.

Fig. 11
figure 11

Example for the use of US in assessment of the radiographically opaque thorax. (a) Chest film revealing reduced translucency of the left hemithorax, with some mediastinal shift to the left and hyperinflation of the right side. (b) Ultrasound of the same patient as Fig. 11a, sagital ventral paramedian views of the left hemithorax: total atelectasis of the left lung is demonstrated, with fluid-filled vessels and fluid-bronchogram, using a parasternal sagital access for lung visualisation

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Some other reported applications are less commonly used in children, partially because these entities are more common in adults (e.g., pleural metastases, peripheral infarction). Other reported applications are not generally accepted or not widely used, e.g., US for diagnoses and follow-up in neonatal hyaline membrane syndrome [59]. Ultrasound may depict pneumothorax using indirect signs such as lack of or inverted movement of the echogenic air-tissue border; however, even if recognised sonographically, this condition usually requires plain film or CT [60].

Other restrictions of US have to be considered: US relies on access via non-calcified and non-aerated tissue to the area of interest, which is restricted particularly in diffuse or central lung problems; thus US is poor in ruling out certain conditions. Ultrasound cannot conspicuously demonstrate a panoramic overview; thus location and assessment of the entire extend of various conditions may be difficult or insufficient, and follow-up may suffer from errors caused by different access and planes. US is relatively investigator dependent; proper equipment as well as training and experience are most important to grant a reliable US diagnosis and useful imaging documentation necessary for communication with clinicians and parents as well as for further treatment decisions and follow-up comparison. An US examination may be time consuming; it usually takes longer to meticulously assess the entire pathology on US than performing a radiograph and/or a chest CT. Furthermore, availability of experienced US for these queries is restricted, as sick children do not adhere to routine working hours and many conditions are presented at night, where dedicated paediatric US is unavailable. All this leads to a rather reluctant use of US in paediatric chest queries not corresponding well with the large US potential.

In conclusion

I want to summarise that US has great potential in many paediatric chest queries. Ultrasound is not invasive, doesn’t use ionising radiation or contrast media, it does not require sedation or anaesthesia, and can readily be applied at the bedside. It can easily be repeated and may offer additional functional information difficult to retrieve by conventional sectional imaging or plain films. All these features should recommend US as a useful additional imaging tool, supplementing radiographs and helping to tailor further sectional imaging if necessary. To ensure diagnostically valuable US, adequate equipment and availability of trained staff should be promoted in order to grant reliable access to this valuable modality for infants and children. With this approach US will become a valued and indispensable additional imaging tool that hopefully will achieve growing acceptance and realistic reimbursement, and thus eventually may find its established role in the imaging algorithm of many paediatric chest conditions.