key: cord-0931322-x1x9c8k9
authors: Millington, Scott J.; Koenig, Seth; Mayo, Paul; Volipcelli, Giovanni
title: How I do it – Lung Ultrasound for Patients with COVID-19 Pulmonary Disease
date: 2020-08-21
journal: Chest
DOI: 10.1016/j.chest.2020.08.2054
sha: 4fcb6233f4e1b5176633e27fbec97ead6dbd0ede
doc_id: 931322
cord_uid: x1x9c8k9

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.

Given the general utility of lung ultrasound (LUS) for the evaluation of respiratory failure in acutely ill 5 patients, it is logical to consider its specific advantages in COVID-19 related pulmonary disease. The 6 authors, representing the extensive experience of the North American and European COVID-19 7 epicenters, present an ultrasound scanning protocol and report on the common associated ultrasound 8 findings. 9 10 11 Case Presentation 12 An obese 62-year-old man with hypertension and type-2 diabetes presents to a New York City hospital 13 with a seven-day history or progressive dyspnea and non-productive cough. On presentation he is 14 hypoxemic (oxygen saturation of 82% on room air) and febrile (38.9 O C), with a normal blood pressure 15 and a heart rate of 115 bpm. His laboratory tests, including COVID-19 testing, are pending. 16 17 18

It is useful for purposes of comparison to summarize the changes expected on chest CT and lung 20 ultrasound (LUS). Findings from three recent Coronavirus outbreaks (SARS [1] , MERS [2] , and COVID-19 21 [3] ) are similar; each is associated with ground-glass opacities (GGO) with or without consolidation with 22 a predilection for the lower lobes, typical peripheral/subpleural locations of GGO lesions, multi-focal and 23 bilateral lung involvement, and the absence of large pleural effusions. One large study [3] reported the 24 following specific patterns in COVID-19 disease: presence of GGO and consolidation (41% of 121 25 patients), presence of GGO alone (34%), presence of consolidation alone (2%), absence of both GGO and 26 consolidation (22%). The disease was bilateral or multifocal in most cases and favored the lower lobes. 27 28

In addition to its diagnostic utility (discussed in detail below) LUS has a potential role in monitoring 29 patients for signs of improvement or deterioration, although the specific details remain unclear at 30 present. Other parts of the point-of-care ultrasound toolkit, such as cardiac or vascular ultrasound, likely 31 also have an important role to play, especially in severely ill patients where diagnostic uncertainty exists. 32

Limitations of LUS generally can be grouped into operator factors (given its operator-dependent nature) 33

and patient factors (with obesity and immobility being particularly relevant). 34 35 36

Scanning Protocol 37

There are different opinions within the ultrasound community with respect to specific scanning 38 protocols. Clinicians who are less familiar with LUS can refer to two related articles published in this 39 issue of CHEST: a hands-on guide to performing basic LUS [4] , and a review of the utility of general LUS 40 in acutely ill patients [5] . Most providers will have access to a lower-frequency transducer, either 41 phased-array ("cardiac") or curvilinear ("abdominal"). Either can be used effectively, depending mostly 42 on user preference. 43 44

Depending on the clinical context, some providers favor a simple 3-point-per-hemithorax sequence, 45 essentially copying the seminal BLUE protocol [6] . Others prefer a more comprehensive scanning 46 protocol such as that described in the 2012 international evidence-based recommendations for point-of-47

care LUS [7] . Specifically for patients with suspected COVID-19 it is appropriate to focus attention on the 48 posterior and dependent lung areas, as the disease tends to manifest itself in these areas which are not 1 well covered by many traditional protocols [3] . The following scanning sequence (see Figure 1 ) is 2 recommended, and other similar protocols exist [8]: 3 1) At the 2 nd intercostal space in the mid-clavicular line, the operator examines the anterior 4 pleural line for lung sliding. Some providers also use the high-frequency linear transducer here 5

to examine pleural line morphology in more detail, although others use the single, lower-6 frequency transducer for the entire exam. 7 2) Using the lower-frequency transducer for the remainder of the exam, the operator examines 8 the intercostal spaces of the anterior area (Zone 1, see Figure 1A ). Steps 2-5 focus on the 9

identification common LUS findings including A-lines, B-lines, pleural effusions, and 10 consolidation. 11

3) The operator examines the intercostal spaces of the upper lateral area (Zone 2, see Figure  12 1B). 13 4) The operator examines the costo-phrenic angle for pleural effusion or dependent areas of 14 consolidation above the diaphragm (see Figure 1B ). 15

5) The patient is placed in the lateral decubitus to scan the posterior thorax. The operator 16 examines the area between the scapula and the spine (Zone 3, see Figure 1C ) and the basal area 17 below the inferior margin of the scapula (Zone 4, see Figure 1C ). 18 6) Additional scans are performed as needed to further characterize local areas of abnormality. 19 20

Given the heterogenous nature of this disease, a systematic examination remains paramount. As many 21

intercostal spaces as possible should be scanned, and each point should be interrogated for a full 22 respiratory cycle. 23 24 25

Lung Ultrasound Findings in Coronavirus Infection 26

The typical LUS findings reported in COVID-19 afflicted patients include [9] (see Figure 2 ): 27

• B-lines -usually multifocal, separated, and confluent -accompanied by segments of irregular 28 pleural line alternating with small peripheral consolidations. B-lines are visualized in various 29

intensities and distributions depending on the severity of illness 30

• Bilateral disease affecting multiple lobes 31

• Areas of patchy B-lines alternating with regular A-lines zones (spared areas or "skip" lesions) 32

• Small peripheral consolidations present in any lung zone, but more common at the lung bases 33

• Less commonly larger consolidations with or without dynamic air bronchograms; large areas of 34 consolidated lung should prompt consideration of a superimposed bacterial pneumonia 35

• Absent or small pleural effusions. 36 37

All of these findings are non-specific, and therefore LUS cannot by itself establish a definitive diagnosis 38 of COVID-19 infection; the same problem applies, of course, to CXR and chest CT findings [10] . The 39

pattern of patchy B-lines is typical for patients with ARDS, for example, and the subpleural 40

consolidations can be found with other viral infections. As such the integration of typical LUS findings 41 with patient history, physical examination, laboratory results, and prevalence of the disease during the 42 pandemic phases is required. A correlation between LUS findings and pathological severity has been 43

proposed [11] , which also highlights the fact that milder cases may present more of a diagnostic 44 challenge. 45 46

The authors have noted an unusual LUS finding that may be more specific to COVID-19: a thick 1 hyperechoic band of confluent B-lines arising from a portion of the pleural line which appears relatively 2 spared (comparatively smooth) [12] [13] . This finding is best appreciated using the convex transducer 3

with the scanning plane orientated along the long axis of an intercostal space (parallel to the ribs), such 4 that a long uninterrupted length of pleura is visualised; note that this is a difference from the transducer 5 orientation preferred by many providers. Some clinicians refer to this finding using the descriptive, but 6 non-standard term "light beam". These areas of hyperechoic confluent B-lines stand out as they often 7

alternate with spared areas of relatively normal lung, seen on ultrasound as A-lines and representing 8 spared areas. "Light beams" commonly move back-and-forth in tune with the respiratory cycle (see 9 Figure 3 and Videos 1, 2, & 3). We speculate that this sign tends to occur in early disease because of the 10 patchy nature of the GGO lesions seen on chest CT, which are concentrated at the lung periphery and 11

subject to respiratory movement. They may evolve, as the disease progresses, towards coalescent B-12

lines associated with pleural line irregularities and small subpleural consolidations. This evolution may 13

correspond to progressive thickening of the interlobular septa (crazy paving as seen on chest CT) and 14 alveolar filling (consolidation as seen on CT). 15 16 17

Lung Ultrasound Disease Patterns 18

The various combinations of signs typically observed in patients with COVID-19 disease allows LUS 19

findings to be clustered into patterns. Each may help differentiate the probability of having the disease, 20

and can be classified as: 21 1) High probability LUS pattern 22

The most typical LUS pattern, as described above, consists of bilateral and multifocal 23 clusters of B-lines alternating with normal lung (spared areas or "skip" lesions), with or 24 without small peripheral consolidations. An associated "light beam" pattern may be present. 25

Increased density of B-lines in posterior and inferior regions is typical. 26

2) Intermediate probability LUS pattern 27

A less typical pattern includes unilateral clusters of B-lines or focal multiple B-lines with or 28 without peripheral consolidations. 29

3) Alternate LUS pattern 30

An isolated large lobar consolidation with air bronchograms, a large pleural effusion, or 31 diffuse and very symmetrical B-lines with a gravity-related distribution are less common in 32 COVID-19 lung disease (being more consistent with bacterial pneumonia, pleural effusion, 33

and cardiogenic pulmonary edema, respectively). These findings alert the clinician to search 34

for an alternate diagnosis. Patients with relatively mild non-respiratory symptoms and no signs of respiratory failure. 1 2) Severe Phenotype 2

Patients with significant dyspnea at rest or on exertion, or signs of respiratory failure. 3 3) Mixed Phenotype 4

Patients with dyspnea or respiratory failure, but with pre-existing significant chronic pulmonary 5 or cardiac disease which may confound their presentation. 6 7 Another related variable to consider is timing of symptom onset; patients with more severe clinical or 8

LUS findings earlier in their disease course may be at higher risk of progression to respiratory failure. 9 10 11 Triage 12

Triaging patients with suspected COVID-19 is a challenge due to the need for rapid decision making in 13 the absence of test results and in the presence of limited resources. Patients must be isolated and 14

personal protective equipment (PPE) donned where uncertainty exists, and decisions regarding 15 admission to hospital and potential treatments must be made quickly and before test results are 16

available. These decisions are particularly challenging in a scenario where patients suspected of COVID-17 19 flock to the emergency department during the height of an outbreak. 18 19

The interface between the patient phenotype (severity of clinical presentation) and the ultrasound 20 pattern may be useful and will be immediately available assuming the presence of providers proficient 21 in LUS. Immediate use of LUS for triage decisions may result in a lower risk of dissemination in crowded 22 emergency departments when compared to the routine use of CXR or CT scan. Combining clinical 23 phenotypes and LUS patterns can guide triage (see Figure 4) signs & symptoms, and may need further investigation by CT scan and confirmation with testing. 45

• An Alternate LUS pattern, with signs such as a large consolidation or pleural effusion, suggests 46

an alternate diagnosis as an explanation for the patient's symptoms. These patients should be 47 isolated until test results are available, admitted to hospital, and treated for their alternate 1 diagnosis. 2

• A Low Probability LUS pattern in association with significant dyspnea or respiratory failure 3

suggests an alternative diagnosis such as pulmonary embolism, asthma, or COPD exacerbation. 4

In doubtful cases with cough and fever, these patients should be isolated until test results are 5 available given the possibility of COVID-19 co-infection without pneumonia. 6 7 For the Mixed Phenotype (patients with respiratory failure and pre-existing pulmonary or cardiac 8 disease): 9

• A High Probability LUS pattern is likely to be related to COVID-19 but must be viewed in the 10 context of an underlying disease which may confound the symptoms and severity of the clinical 11

presentation. 12

• The Intermediate Probability and Alternative LUS patterns, as described above, require 13

integration of LUS findings with current clinical scenario in the context of the patient's comorbid 14 medical conditions; here great uncertainty with respect to the possibility of COVID-19 remains 15

and CT scan may be crucial. 16

• A Low probability LUS pattern is unlikely to be found in patients with significant pre-existing 17 pulmonary or cardiac disease. 18 19 20

Conclusion 21

While the specific role for LUS in the management of COVID-19 disease is still evolving, its utility in the 22 management of patients with respiratory failure in general is very well established. Given the severity of 23 illness associated with this particular pathogen and the need for strict isolation protocols, there is 24 evidence to suggest that LUS will emerge as the best available imaging modality for these patients. 25 26 27 

Significant dyspnea or signs of respiratory failure.

Dyspnea or respiratory failure, but with confounding pre-existing lung or heart disease. 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.

Suggests an alternative diagnosis to explain the patient's symptoms. These patients should be isolated until test results are available, admitted to hospital, and treated for their alternate diagnosis.

Uncertain; requires integration of LUS findings with current clinical scenario in the context of the patient's comorbid medical conditions, CT scan may be helpful.

A normal or near-normal exam; generalized bilateral A-lines with lung sliding.

Rules out severe COVIDrelated lung disease but not the possibility of infection with the virus itself; these patients can be considered for discharge to home quarantine.

Suggests an alternative diagnosis such as pulmonary embolism, asthma, or COPD exacerbation; these patients should be isolated until test results are available.

Unlikely to be found in patients with significant pre-existing pulmonary or cardiac disease.

Imaging in Severe Acute Respiratory Syndrome (SARS)

Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Infection: Chest CT Findings

Chest CT Findings in Coronavirus Disease-19 (COVID-19): Relationship to Duration of Infection

Better with Ultrasound: Thoracic Ultrasound

Lung Ultrasound for Respiratory Failure in Acutely Ill Patients: A Review

The BLUE-points: three standardized points used in the BLUEprotocol for ultrasound assessment of the lung in acute respiratory failure

International evidence-based recommendations for point-of-care lung ultrasound

Proposal for International Standardization of the Use of Lung Ultrasound for Patients With COVID -19

Findings of lung ultrasonography of novel corona virus pneumonia during the 2019-2020 epidemic

Chest CT findings of COVID-19 pneumonia by duration of symptoms

Histological-ultrasonographical correlation of pulmonary involvement in severe COVID-19

Sonographic signs and patterns of COVID-19 pneumonia

What's new in lung ultrasound during the COVID-19 pandemic