14 Jul The “pandemic” increase in lung ultrasound use in response to Covid-19: can we complement computed tomography findings? A narrative review
Coronavirus disease of 2019 (COVID-19) is a highly infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which has rapidly spread to a global pandemic in March 2020.
This emergency condition has been putting a severe strain on healthcare systems worldwide, and a prompt, dynamic response is instrumental in its management.
While a definite diagnosis is based on microbiological evidence, the relationship between lung ultrasound (LU) and high-resolution computed tomography (HRCT) in the diagnosis and management of COVID-19 is less clear.
Lung ultrasound is a point-of-care imaging tool that proved to be useful in the identification and severity assessment of different pulmonary conditions, particularly in the setting of emergency and critical care patients in intensive care units; HRCT of the thorax is regarded as the mainstay of imaging evaluation of lung disorders, enabling characterization and quantification of pulmonary involvement.
Aims of this review are to describe LU and chest HRCT main imaging features of COVID-19 pneumonia, and to provide state-of-the-art insights regarding the integrated role of these techniques in the clinical decision-making process of patients affected by this infectious disease.
In the ongoing battle against the disease caused by SARS-CoV-2 (COVID-19), which first broke out in the city of Wuhan, China, in December 2019, lung ultrasound (LU)  has quickly been recognized as a useful tool in the diagnosis and monitoring of the disease .
Ultrasound cannot replace lung computed tomography (CT) when examining the whole lung to choose a ventilator strategy , but point-of-care ultrasound (POCUS) may complement CT thanks to ease of access and general safety.
In this review, we summarize the main LU findings in COVID-19 pneumonia next to the equivalent CT signs , in the hopes that a correlation can be established to facilitate patient care. In clinical practice, the two imaging modalities can be integrated with great benefits for both patients and clinicians. Although limited in the extent of lung tissue it can explore, LU is particularly advantageous when confronting a COVID-19 outbreak: for one, ventilated patients need to be transferred to a CT suite, which can be outright dangerous in the face of severely impaired gas exchange commonly seen in COVID-19 intensive care unit (ICU) patients.
We are not yet aware of LU signs specific for COVID-19, but signs of interstitial pneumonia are well recognized and have been found to be applicable in these cases, with some exhibiting high sensitivity [5, 6]. Additionally, it is now sufficiently clear that LU outperforms plain chest radiography in terms of sensitivity for acute respiratory symptoms in critical illness [7, 8].
A reasonable approach may be to perform CT scans on ICU admission to finalize diagnosis and to better inform the choice of ventilation (lung phenotyping) ; in order to reduce radiation and viral exposure, it could be repeated after a reasonable interval of time for prognostic information, whereas POCUS could be used to reduce ionizing radiation load and device contamination in many situations where it has been shown to be superior to chest x-ray and (in selected cases) as useful as CT . Another setting in which LU is becoming essential is that of community outreach by specialized teams screening residents of nursing homes and long-term care facilities, which may have acted as a reservoir for SARS-CoV-2 .
Conversely, LU may not explore the entirety of the organ, and one should always consider CT when point-of-care monitoring fails to explain the current clinical respiratory status, especially in COVID-19, where thrombotic complications are increasingly found to be pivotal in the disease . The aim of this review is thus to help physicians become familiar with LU and CT imaging in COVID-19.
Lung ultrasound and COVID-19
Patients with interstitial syndromes usually display two types of artifacts.
A-lines are the ‘default’ artifacts in healthy lung tissue, caused by soundwaves reverberating between pleura and the transducer, as the air-tissue interface reflects almost all the ultrasound packets. The sliding motion of the hyperechoic line in the near field depicts the movement of visceral over parietal pleural.
The presence of A-lines and lung sliding signifies normal lung aeration (Fig. 1 )
Anterior parasagittal lung ultrasound scan of the thorax. The parietal and visceral pleura appear as a hyperechoic line with sliding movements (also see Additional file 1). A lines are thought to be mirror artifacts from the near-total ultrasound reflection by the pleura-alveolar gas interface
B-lines. Hyperechoic artifacts descending from the pleural line to the bottom of the screen are called “B lines” (black asterisks); by definition, a B line obscures any A line along its path. Two B lines per scan field are considered normal; ≥ 3 lines are associated with varying degrees of interstitial syndrome
The clinical significance of B-lines depends mostly on quality and quantity: ≤ 2 B-lines per intercostal space, interspersing A-line, and a sliding pleural line rule out pneumothorax and are considered normal variation.
The pleural line is normally thin and bright but, when inflamed, it can become thickened and less mobile, with B-lines arising from it and arcing slowly. The pleural line can also be interrupted by lung consolidation and loss of aeration (the “shred sign”) . At the beginning of lung involvement in COVID-19, B-lines (with lung sliding) are distributed heterogeneously between spared regions of A-lines (Fig. 3).
As the disease progresses, lung density increases, as does the amount of B-lines, leading to coalescence of the artifacts into “glass-rockets” and then “white lung” (Figs. 3 and 4, respectively; see also Additional file 3: Clip S3 and Additional file 4: Clip S4), equivalent ground-glass opacities (GGO) in CT scans .
Amid a pandemic with a very high prevalence of the disease, high density of B-lines with spared areas and lung sliding plus fever and cough is high suspicious for COVID-19 infection, and these patients should be managed accordingly [15, 16]. Glass rockets or white lung are typically associated with impaired oxygenation requiring supplemental oxygen.
Confluent B-lines. Multiple confluent B-lines (asterisks) and occupying ≥ 50% of the field of view define the “rocket launch” sign or “glass rockets.” This is associated with more overt interstitial syndrome. Additional file 1: Clip S1: Anterior parasagittal scan of the thorax. The parietal and visceral pleura appear as a hyperechoic line. Pleural sheaths are seen sliding with respiration
White lung. In this parasagittal scan, the whole intercostal space is occupied by continuous hyperechoic artifact commonly referred to as “white lung.” The pleural line also appears coarser and thicker than normal. This image is associated with advanced interstitial syndrome and may precede complete loss of aeration (consolidation)
Finally, in advanced disease, lung density further increases as alveoli fill up with inflammatory cells and Lung ultrasound findings in patients with COVID-19 pneumonia byproducts, with loss of aeration and a corresponding LU aspect called “tissue-like” (Fig. 5).
This is equivalent to consolidation as seen in CT scans. The appearance of consolidations in LU is similar to that of liver tissue, with hyperechoic inclusions corresponding to distal bronchi which may or may not be filled with secretions .
Subpleural consolidations and “light beam”. Two artifacts frequently seen in COVID-19 with significant respiratory symptoms: small subpleural consolidation (asterisk), with white lung-like artifact projecting from its interface with aerated lung (between black arrows); and a “light beam”, a hyperechoic artifact (between white arrows), also similar in quality to white lung, but arising from a discrete region of normal pleura.
The light beam is so called also because it is “turned off and on” (i.e., disappears and reappears) repeatedly, even in a single respiratory cycle.
What is new in this context?
Recently, Volpicelli et al. have described some aspects of B-lines that seem to increase the diagnostic probability in patients suspected of COVID-19 pneumonia , in combination with clinical phenotype, blood tests and nasal-pharyngeal swab.
They report on a sonographic sign named “light beam” and described as a shining vertical band artifact arising from a wide portion of a regular pleura, as opposed to the discrete points of origin of B-lines. The artifact is thought to be present in the earlier phase of viral spread in the peripheral lung and associated with the early GGO alterations visible at CT scan. This sign has also been described by Huang et al. in patients with COVID-19 infection as a “waterfall” sign . In COVID-19, the light beam artifact is typically interspersed among areas of normal lung aeration or discrete B-lines, often alternating with areas of pleural line irregularity and peripheral consolidations.
In COVID-19, two pathological phenotypes have been described. One is the L-type, with normal or minimally reduced respiratory system compliance; these patients have been dubbed by some Authors as “happy hypoxic”, and a prospective multicenter study is currently investigating whether the light beam sign could be an early sign of disease in these cases.
On CT, they show diffuse infiltrates but a low margin of recruitability (hence the name), defined as a relatively minor volume of de-aerated lung tissue . The H-phenotype is characterized by low- to very low respiratory system compliance with high potential for recruitment with higher mean airway pressures; CT of these patients typically shows extensive consolidation with or without superimposed bacterial pneumonia. While L-type COVID-19 is intuitively characterized by the presence of LU signs such as those we described above (a multicenter study is ongoing to confirm this hypothesis), LU of H-type COVID-19 might have more in common with bacterial pneumonia and atelectasis. On CT, up to three different profiles can be described according to the distribution of consolidations .
From their characteristics, it has been proposed that different phenotypes require distinct respiratory management strategies, based on recruitment potential . However, not all experts concur with this view, promoting instead the concept of a continuous disease which may worsen with mechanical ventilation itself and/or opportunistic infection .
What is known about LU?
Certain characteristics of B-lines can help rule out COVID-19 infection, for example when B-lines are unilateral, which is more typical of initial pneumonia of likely bacterial origin, although underlying COVID-19 pneumonia cannot be ruled out : theoretically, H-type COVID-19 pneumonia might share these features on LU.
A unilateral consolidation within a large pleural effusion suggests bacterial pneumonia rather than COVID-19 pneumonia . Pleural effusion is a well-known sign that appears as a hypo- or anechoic space in LU, distributed in gravity-dependent fashion [23, 24]. Pleural effusion is easy to see, and it may be possible to be estimate its volume with simple calculations (Balik formula) .
Sometimes septa can be seen floating in effusions, which is more typical of bacterial or fungal infection. However, in COVID-19, we have observed that large pleural effusions are rarely present and an alternative diagnosis, or superimposed infection, should be considered when confronted with such sign.
Lung ultrasound score (LUS)
When performing LU, it is customary to divide the chest into 8 to 16 regions. We will describe an approach where the chest is divided into 12, defined by the intersections of the anterior and posterior axillary lines with a transverse plane passing through both nipples (Fig. 6). These regions can be scanned with different probes, depending on personal experience and preference, the most common being convex low-frequency and phased array (echocardiography) transducers .
Representation of the 6-zone model for lung ultrasound score (see Ref. ). The parasagittal lines are the midclavicular, anterior and posterior axillary lines; the transverse line is at the 4th intercostal space, roughly equivalent to hilar lines
Lung ultrasound score is a system in which each of 12 lung zones is assigned points, which are then added up . One point is assigned to zones with A-lines and pleural sliding, or ≤ 2 B-lines; 1 point is for ≥ 3 well-spaced B-lines (interstitial syndrome); and 2 points are calculated for coalescent B-lines or “glass-rockets”—equivalent to GGO in CT; finally, consolidation with “tissue like-sign” has a score of 3.
Therefore, the total score may range between 0 (normal lungs) and 36, in the worst-case scenario of completely de-aerated lungs . We do not know how the “light beam” sign or small superficial lung consolidations may affect this score.
Diagnostic performance of LU
Ultrasound distinction between acute cardiogenic pulmonary edema and acute respiratory distress syndrome (ARDS) in a critically ill patient can be difficult . As is the case in every interstitial syndrome, non-infectious causes of pulmonary edema are always a differential diagnosis [28, 29].
The presence of bilateral B lines is associated with an interstitial syndrome, as previously reported , but it is poorly specific (while sensitivity is close to 100%). On the one hand, the presence of some ultrasound signs such as abnormalities of the pleural line, the reduction of pleural sliding, interspersed sparing areas, and the presence of consolidations can suggests ARDS over cardiogenic pulmonary edema (sensitivity 83–100% and specificity 45–100%) .
On the other hand, evidence on the diagnostic value of LU in ARDS is still very discordant. Diagnostic accuracy of LU for interstitial syndrome suffers considerably from variability between different research groups [area under the curve (AUC) of the receiver operating characteristic curve (ROC) from 85 to 95%] [31, 32]. The diagnosis of pneumonia by detection of lung consolidations (typical of bacterial pneumonia) was found to have sensitivity and specificity approaching those of CT (up to 95% and 91%, respectively).
Ultimately, the diagnostic accuracy of LU seems to be greater than 90% [24, 25]. In viral pneumonia, LU has shown good sensitivity (94.1%) but inferior specificity (84.8%), with positive and negative predictive values of 86.5% and 93.3%, respectively . Again, signs of interstitial syndromes can be present in a host of different conditions. , and at the time of this writing only anecdotal reports have been published for LU diagnosis of COVID-19.