Scott J. Millington, MD, Seth Koenig, MD, Paul Mayo, MD, Giovanni Volipcelli, MD

Chest Journal

Abstract

Given the general utility of lung ultrasound (LUS) for the evaluation of respiratory failure in acutely ill patients, it is logical to consider its specific advantages in COVID-19 related pulmonary disease.

The authors, representing the extensive experience of the North American and European COVID-19 epicenters, present an ultrasound scanning protocol and report on the common associated ultrasound findings.

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Case Presentation

An obese 62-year-old man with hypertension and type-2 diabetes presents to a New York City hospital with a seven-day history or progressive dyspnea and non-productive cough.

On presentation he is hypoxemic (oxygen saturation of 82% on room air) and febrile (38.9 C), with a normal blood pressure and a heart rate of 115 bpm. His laboratory tests, including COVID-19 testing, are pending.

Utility of LUS in COVID-19 infection

It is useful for purposes of comparison to summarize the changes expected on chest CT and lung ultrasound (LUS). Findings from three recent Coronavirus outbreaks (SARS [1], MERS [2], and COVID-19 [3]) are similar; each is associated with ground-glass opacities (GGO) with or without consolidation with a predilection for the lower lobes, typical peripheral/subpleural locations of GGO lesions, multi-focal and bilateral lung involvement, and the absence of large pleural effusions.

One large study [3] reported the following specific patterns in COVID-19 disease: presence of GGO and consolidation (41% of 121 patients), presence of GGO alone (34%), presence of consolidation alone (2%), absence of both GGO and consolidation (22%).

The disease was bilateral or multifocal in most cases and favored the lower lobes.

In addition to its diagnostic utility (discussed in detail below) LUS has a potential role in monitoring patients for signs of improvement or deterioration, although the specific details remain unclear at present.

Other parts of the point-of-care ultrasound toolkit, such as cardiac or vascular ultrasound, likely also have an important role to play, especially in severely ill patients where diagnostic uncertainty exists.

Limitations of LUS generally can be grouped into operator factors (given its operator-dependent nature) and patient factors (with obesity and immobility being particularly relevant).

Scanning Protocol

There are different opinions within the ultrasound community with respect to specific scanning protocols. Clinicians who are less familiar with LUS can refer to two related articles published in this issue of CHEST: a hands-on guide to performing basic LUS [4], and a review of the utility of general LUS in acutely ill patients [5].

Most providers will have access to a lower-frequency transducer, either phased-array (“cardiac”) or curvilinear (“abdominal”). Either can be used effectively, depending mostly on user preference.

Depending on the clinical context, some providers favor a simple 3-point-per-hemithorax sequence, essentially copying the seminal BLUE protocol [6]. Others prefer a more comprehensive scanning protocol such as that described in the 2012 international evidence-based recommendations for point-of48 care LUS [7].

Specifically for patients with suspected COVID-19 it is appropriate to focus attention on the posterior and dependent lung areas, as the disease tends to manifest itself in these areas which are not well covered by many traditional protocols [3]. The following scanning sequence (see Figure 1) is recommended, and other similar protocols exist [8]:

1) At the 2nd 4 intercostal space in the mid-clavicular line, the operator examines the anterior pleural line for lung sliding. Some providers also use the high-frequency linear transducer here to examine pleural line morphology in more detail, although others use the single, lower frequency transducer for the entire exam.

2) Using the lower-frequency transducer for the remainder of the exam, the operator examines the intercostal spaces of the anterior area (Zone 1, see Figure 1A).  Steps 2-5 focus on the identification common LUS findings including A-lines, B-lines, pleural effusions, and consolidation.

3) The operator examines the intercostal spaces of the upper lateral area (Zone 2, see Figure1B).

4) The operator examines the costo-phrenic angle for pleural effusion or dependent areas of consolidation above the diaphragm (see Figure 1B).

5) The patient is placed in the lateral decubitus to scan the posterior thorax. The operator examines the area between the scapula and the spine (Zone 3, see Figure 1C) and the basal area below the inferior margin of the scapula (Zone 4, see Figure 1C).

6) Additional scans are performed as needed to further characterize local areas of abnormality.

Given the heterogenous nature of this disease, a systematic examination remains paramount. As many intercostal spaces as possible should be scanned, and each point should be interrogated for a full respiratory cycle.

Lung Ultrasound Findings in Coronavirus Infection

The typical LUS findings reported in COVID-19 afflicted patients include [9] (see Figure 2):

• B-lines – usually multifocal, separated, and confluent – accompanied by segments of irregular
pleural line alternating with small peripheral consolidations. B-lines are visualized in various intensities and distributions depending on the severity of illness

• Bilateral disease affecting multiple lobes

• Areas of patchy B-lines alternating with regular A-lines zones (spared areas or “skip” lesions)

• Small peripheral consolidations present in any lung zone, but more common at the lung bases

• Less commonly larger consolidations with or without dynamic air bronchograms; large areas of consolidated lung should prompt consideration of a superimposed bacterial pneumonia

• Absent or small pleural effusions.

All of these findings are non-specific, and therefore LUS cannot by itself establish a definitive diagnosis of COVID-19 infection; the same problem applies, of course, to CXR and chest CT findings [10]. The pattern of patchy B-lines is typical for patients with ARDS, for example, and the subpleural consolidations can be found with other viral infections.

As such the integration of typical LUS findings with patient history, physical examination, laboratory results, and prevalence of the disease during the pandemic phases is required. A correlation between LUS findings and pathological severity has been proposed [11], which also highlights the fact that milder cases may present more of a diagnostic challenge.

The authors have noted an unusual LUS finding that may be more specific to COVID-19: a thick hyperechoic band of confluent B-lines arising from a portion of the pleural line which appears relatively spared (comparatively smooth) [12] [13].

This finding is best appreciated using the convex transducer with the scanning plane orientated along the long axis of an intercostal space (parallel to the ribs), such that a long uninterrupted length of pleura is visualised; note that this is a difference from the transducer orientation preferred by many providers. Some clinicians refer to this finding using the descriptive, but non-standard term “light beam”.

These areas of hyperechoic confluent B-lines stand out as they often alternate with spared areas of relatively normal lung, seen on ultrasound as A-lines and representing spared areas. “Light beams” commonly move back-and-forth in tune with the respiratory cycle (see Figure 3 and Videos 1, 2, & 3).

We speculate that this sign tends to occur in early disease because of the patchy nature of the GGO lesions seen on chest CT, which are concentrated at the lung periphery and subject to respiratory movement. They may evolve, as the disease progresses, towards coalescent B13 lines associated with pleural line irregularities and small subpleural consolidations.

This evolution may correspond to progressive thickening of the interlobular septa (crazy paving as seen on chest CT) and alveolar filling (consolidation as seen on CT).

Lung Ultrasound Disease Patterns

The various combinations of signs typically observed in patients with COVID-19 disease allows LUS findings to be clustered into patterns. Each may help differentiate the probability of having the disease, and can be classified as:

1) High probability LUS pattern

The most typical LUS pattern, as described above, consists of bilateral and multifocal clusters of B-lines alternating with normal lung (spared areas or “skip” lesions), with or without small peripheral consolidations. An associated “light beam” pattern may be present. Increased density of B-lines in posterior and inferior regions is typical.

2) Intermediate probability LUS pattern

A less typical pattern includes unilateral clusters of B-lines or focal multiple B-lines with or without peripheral consolidations.

3) Alternate LUS pattern

An isolated large lobar consolidation with air bronchograms, a large pleural effusion, or diffuse and very symmetrical B-lines with a gravity-related distribution are less common in COVID-19 lung disease (being more consistent with bacterial pneumonia, pleural effusion, and cardiogenic pulmonary edema, respectively). These findings alert the clinician to search for an alternate diagnosis.

4) Low probability LUS pattern

A generalized bilateral A-line pattern with lung sliding indicates normal lung aeration. Significant dyspnea presenting with this ultrasound pattern requires consideration of an alternate diagnosis other than COVID-19. This pattern is also seen in pulmonary embolism, potentially important due to the association between COVID-19 infection and thromboembolic disease [14]. In patients who are well, a normal LUS pattern does not exclude infection with COVID-19 without pulmonary involvement.

Clinical COVID-19 Patient Phenotypes

Correlation of the LUS pattern with clinical information is crucial to increase diagnostic confidence while test results are pending, and the patient presentations can be divided as follows:

1) Mild Phenotype: Patients with relatively mild non-respiratory symptoms and no signs of respiratory failure.

2) Severe Phenotype: Patients with significant dyspnea at rest or on exertion, or signs of respiratory failure.

3) Mixed Phenotype: Patients with dyspnea or respiratory failure, but with pre-existing significant chronic pulmonary or cardiac disease which may confound their presentation.

Another related variable to consider is timing of symptom onset; patients with more severe clinical or LUS findings earlier in their disease course may be at higher risk of progression to respiratory failure.

Triage

Triaging patients with suspected COVID-19 is a challenge due to the need for rapid decision making in the absence of test results and in the presence of limited resources.

Patients must be isolated and personal protective equipment (PPE) donned where uncertainty exists, and decisions regarding admission to hospital and potential treatments must be made quickly and before test results are available.

These decisions are particularly challenging in a scenario where patients suspected of COVID18 19 flock to the emergency department during the height of an outbreak.

The interface between the patient phenotype (severity of clinical presentation) and the ultrasound pattern may be useful and will be immediately available assuming the presence of providers proficient in LUS. Immediate use of LUS for triage decisions may result in a lower risk of dissemination in crowded emergency departments when compared to the routine use of CXR or CT scan.

Combining clinical phenotypes and LUS patterns can guide triage (see Figure 4), as follows:

For the Mild Phenotype (patients with mild symptoms and no signs of respiratory failure):

• A High Probability LUS pattern indicates a high probability of COVID-19 pneumonia. Testing should be performed, but a negative result would be at high risk of representing a false negative.

• An Intermediate Probability LUS pattern may define a group of patients where close monitoring, whether at home or in the hospital, should be considered.

• An Alternate LUS pattern, with signs such as a large consolidation or pleural effusion, suggests an alternative diagnosis to explain the patient’s symptoms. These patients should be isolated until test results are available while management of the alternate diagnosis is undertaken, and a lower threshold for admission to hospital applied.

• A Normal LUS pattern rules out severe COVID-related lung disease but not the possibility of infection with the virus itself; these patients can be considered for discharge to home quarantine and monitoring while test results are pending, assuming they are otherwise well.

For the Severe Phenotype (patients with signs of significant dyspnea or respiratory failure, all of whom
should be considered for hospital admission):

• A High Probability LUS pattern establishes a high probability of COVID-19 pneumonia. Testing should be performed, but here again a negative result may well represent a false negative.

• An Intermediate Probability LUS pattern presents a mismatch between LUS finding and patient signs & symptoms, and may need further investigation by CT scan and confirmation with testing.

• An Alternate LUS pattern, with signs such as a large consolidation or pleural effusion, suggests an alternate diagnosis as an explanation for the patient’s symptoms. These patients should be isolated until test results are available, admitted to hospital, and treated for their alternate diagnosis.

• A Low Probability LUS pattern in association with significant dyspnea or respiratory failure suggests an alternative diagnosis such as pulmonary embolism, asthma, or COPD exacerbation.

In doubtful cases with cough and fever, these patients should be isolated until test results are available given the possibility of COVID-19 co-infection without pneumonia.

For the Mixed Phenotype (patients with respiratory failure and pre-existing pulmonary or cardiac disease):

• A High Probability LUS pattern is likely to be related to COVID-19 but must be viewed in the context of an underlying disease which may confound the symptoms and severity of the clinical presentation.

• The Intermediate Probability and Alternative LUS patterns, as described above, require  integration of LUS findings with current clinical scenario in the context of the patient’s comorbid medical conditions; here great uncertainty with respect to the possibility of COVID-19 remains and CT scan may be crucial.

• A Low probability LUS pattern is unlikely to be found in patients with significant pre-existing pulmonary or cardiac disease.

Conclusion

While the specific role for LUS in the management of COVID-19 disease is still evolving, its utility in the management of patients with respiratory failure in general is very well established.

Given the severity of illness associated with this particular pathogen and the need for strict isolation protocols, there is evidence to suggest that LUS will emerge as the best available imaging modality for these patients.

Additional information

References

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