key: cord-0936466-pg9cehnt
authors: Koenig, Seth; Mayo, Paul; Volipcelli, Giovanni; Millington, Scott J.
title: Lung Ultrasound for Respiratory Failure in Acutely Ill Patients: A Review
date: 2020-08-22
journal: Chest
DOI: 10.1016/j.chest.2020.08.2052
sha: 1ee6d1ed2895d622bb759864b2b956968c72f4df
doc_id: 936466
cord_uid: pg9cehnt

Abstract Lung ultrasound (LUS), an imaging modality quickly performed, interpreted, and integrated by the treating physician at the bedside, is a particularly useful tool for acutely ill patients. In evaluating a patient with respiratory failure in the intensive care unit or emergency department, LUS is superior to chest x-ray and generally comparable to computerized tomography, reducing the need for patient transport and radiation exposure. This article will provide a concise review of LUS as it pertains to respiratory failure in general and will include examples of relevant ultrasound images and video clips from critically ill patients.

Lung Ultrasound for Respiratory Failure in Acutely Ill Patients: A Review 10 11 12 13 14 Running Title: 15

Lung Ultrasound Review 16 17 18 19 Seth Koenig, MD 20 Montefiore Medical Center / Albert Einstein College of Medicine 21 New York, NY USA 22 23 Paul Mayo, MD 24 Long Island Jewish Medical Center 25

New York, NY USA 26 27 Giovanni Volipcelli, MD 28 San Luigi Gonzaga University Hospital 29 Torino, Italy 30 31 Scott J. Millington, MD 32 University of Ottawa / The Ottawa Hospital 33

Ottawa, ON Canada 34 35 Corresponding Author: 36 Seth Koenig, MD 37 rectones@yahoo.com 38 39 Lung ultrasound (LUS) is a useful imaging modality for managing critically ill patients with respiratory 15 failure due to its favorable diagnostic performance characteristics and overall ease of use. It is superior 16 to physical examination and chest x-ray (CXR) for the diagnosis and evaluation of many respiratory 17 conditions that are commonly encountered in the intensive care unit (ICU) or emergency department 18 (ED) [1] [2] [3] , and it generally performs comparably to computed tomography (CT) [4] [5] [6] . As a test 19 performed by the clinician at the point of care it is fast, safe, and efficient with modern ultrasound 20 machines being portable, widely available, inexpensive, and easy to use. With the onset of the COVID- 19 21 pandemic, erstwhile resource-rich healthcare systems have been stressed by a major surge in 22 operational requirements, further highlighting the utility of ultrasound in reducing use of CXR and CT 23 resources [7] . 24 25 This review will provide an update on the utility of LUS for the evaluation of respiratory failure in acutely 26 ill patients. Clinicians with limited experience in performing LUS should consult the companion "Better 27

with Ultrasound" review, published in this issue of CHEST [8] , which serves as an introductory primer. 28 Providers particularly interested in the specific applications of LUS for patients with COVID-19 should 29

consult the companion article on that subject, also published in this issue of CHEST [9] . While the focus 30 here is on lung imaging, the complimentary nature of point-of-care ultrasound should not be forgotten; 31 in many instances cardiac, abdominal, and deep vein studies will increase the diagnostic yield of LUS 32 [10] . 33 34 35 Lung Ultrasound Technique 36

The general principles regarding transducer selection, orientation, patient positioning, machine setup, 37 and image capture are outlined in detail in the companion "Better with Ultrasound" review [8] . 38 39 Transducer selection: There is significant debate within the ultrasound community regarding the optimal 40 transducer for lung imaging. Most providers recommend a lower frequency transducer as their primary 41 tool, choosing between a convex transducer (commonly used in abdominal imaging and offering the 42 ability to visualize a large portion of the lung surface, offering a rapid examination of the whole chest) 43

and a phased-array transducer (commonly used in cardiac imagining and offering a smaller footprint, 44 enabling easier access to the intercostal spaces). Probe selection is determined primarily by availability 45 and operator preference. Interestingly, some pathological findings such as B-lines (see below) appear 46 slightly different depending on which lower frequency transducer is selected, due to differences in 47 lateral resolution. Many of the classic LUS findings were originally described using a microconvex 48 transducer, but this type of transducer is less commonly used by most ultrasound providers. A higher 1 frequency linear probe (commonly used for guidance of venous access and detection of deep vein 2 thrombosis) has potential applications for detailed examinations of pleural line morphology. 3 4 Patient positioning: Patients, especially those who are critically ill, are generally examined in the supine 5 position, either flat or with the head-of-bed slightly elevated. The patient's arms are positioned such 6 that access to the lateral thorax is unimpeded, and under ideal circumstances they can be turned to the 7 left and right lateral decubitus positions during the exam to facilitate examination of the posterior lung 8 aspects. 9 10

Machine setup: Most modern ultrasound machines now possess a specific "lung" setting, which should 11 be used regardless of which transducer is deployed. For older machines, the "abdominal" setting is a 12 generally acceptable alternative. In all cases, but especially considering the current COVID-19 situation, 13 great attention must be paid to infection control practices. Deference should be paid to established local 14 protocols for sheathing and cleaning machines and transducers. 15 16 Image capture: Scanning depth will vary based on patient body habitus, but a starting depth of 8-10 cm 17

is reasonable for either lower-frequency transducer. Gain should be adjusted such that it is uniform 18 throughout the entire scanning depth. Too much gain, a common error for beginners, can falsely 19

emphasize certain findings such as B-lines. Study archiving is essential for quality assurance, safety, and 20 later scientific study; the recording of video clips (or still images where applicable) is strongly 21 recommended. 22 23 Transducer orientation: Some providers, typical those who favor the large convex transducer, advocate 24 for a longitudinal orientation where the transducer is parallel to the ribs. Those more accustomed to 25 using the phased-array transducer may prefer an oblique orientation with the probe perpendicular to 26 the ribs, yielding the familiar image of two ribs casting acoustic shadows and the pleural line in between. 27 28 29 Scanning Protocol 30

There is disagreement within the ultrasound community with respect to specific scanning protocols. 31 Some providers favor a simple 3-point-per-hemithorax sequence, essentially copying the seminal BLUE 32

protocol [11] intended for critically ill patients with severe dyspnea. Others prefer a more 33 comprehensive scanning protocol such as that described in the 2012 international evidence-based 34

recommendations for point-of-care LUS [12] , arguably more applicable to a broader group of patients 35 with less severe symptoms in clinical environments outside the ICU. Regardless of the scanning protocol 36 selected, an examination which is both flexible and systematic is recommended, especially for 37

conditions like COVID-related lung disease which may present with heterogenous findings. 38 39 A basic 3-point scanning sequence [11] would include (see Figure 1 ): 40 1) At the 2nd intercostal space in the mid-clavicular line, the operator examines the anterior 41 pleural line for lung sliding. Some providers use the high-frequency linear transducer here to 42 examine pleural line morphology in detail. Switching to a lower-frequency probe for the 43 remainder of the exam, the operator examines this same location to identify common LUS 44 findings such as A-lines and B-lines. 45 2) At the 5 th or 6 th intercostal space in the lateral-clavicular line, the lower-frequency probe is 46 applied to identify common LUS findings such as A-lines and B-lines. 47

3) At the posterior-axillary line just above the level of the diaphragm, the lower-frequency probe is 1 again applied. Here the particular focus is determining the presence or absence of lung 2 consolidation or pleural effusion. 3 4 Providers should be prepared to deviate from any chosen protocol in response to pathology detected in 5 a given view. More elaborate protocols range from four-points (per hemithorax) [12] to six-points [13] 6 and beyond. A specific protocol for COVID-related disease is proposed in the accompanying article [9] . 7 8 9 LUS for the Evaluation of Respiratory Failure in the ICU 10 Most imaging modalities, including LUS, CXR, and CT, share a common weakness: the resulting images 11 have no utility until they are integrated with clinical information to generate a diagnosis and 12 management plan. With LUS the bedside clinician is responsible for all aspects, from image acquisition 13

to image interpretation, and from clinical integration to action at the bedside. 14 15

Chest CT has the advantage of excellent image quality, but is burdened by major disadvantages including 16 need for patient transport, radiation exposure, and the inability to perform frequent repeat 17 assessments; this leaves CXR and LUS as the two practical alternatives for most routine ICU imaging, 18 particularly for unstable patients. These two modalities have been compared in evaluating a variety of 19 causes of respiratory failure common to critically ill patients; LUS has been shown to be more sensitive 20

than CXR for the assessment of acute dyspnea, heart failure, adult respiratory distress syndrome (ARDS), 21 pneumonia, and pneumothorax [ Limitations associated with LUS relate primarily to operator factors (as an operator-dependent skill 33 where training and experience are important) and patient factors (where elements such as obesity and 34

immobility can make performing exams difficult). 35 36 37 Common Clinical Questions 38 In performing LUS, clinicians commonly consider questions such as: 39 40 1) Can I quickly rule-out a pneumothorax? 41

Ultrasound of the normally aerated lung will show the pleura line moving with the respiratory or 42 cardiac cycle (lung sliding and lung pulse, respectively), except when the pathological presence 43 of air drives the two pleural layers apart and impedes ultrasound transmission. The presence of 44 lung sliding, a lung pulse, or B-lines achieves the goal of ruling out a pneumothorax at the point 45 of transducer contact by establishing the absence of intervening air (see Video 1) . For lung 46 sliding in particular, a steady hand is important to avoid a false positive result. 47 48 How this information is integrated will depend on the specific clinical scenario at hand. For a 1 patient in shock, the presence of lung sliding, a lung pulse, or B-lines at the most anterior point 2 bilaterally (often the 2 nd intercostal space in the mid-clavicular line is used) would be enough to 3 rule out a large or tension pneumothorax as a cause of hemodynamic instability. When 4 searching for a smaller, more localized pneumothorax a more thorough exam will be required; 5

in such cases detection of a lung "point" [30] confirms with high specificity the diagnosis of 6

pneumothorax. The specific location of the lung point can also facilitate the estimation of the 7 degree of lung collapse [31] . 8 9 2) Is there evidence of an interstitial syndrome? 10 Integrating the number, pattern, and density of B-lines (see Video 2) into the overall clinical 11 presentation can aid in determining both etiology and severity, remaining mindful that 12

conditions including ARDS, pneumonia, cardiogenic pulmonary edema, lung contusion, lung 13 infarction, chronic interstitial lung disease, and lymphangitic carcinomatosis (among others) can 14

all manifest similar LUS findings [32] . Closer examination of the pleura line morphology, in the 15 presence of B-lines, may be useful in distinguishing cardiogenic from non-cardiogenic pulmonary 16 edema [33] . 17 18

The distribution and intensity of B-lines, combined with relevant clinical information, can be 19

very helpful in developing a differential diagnosis. In cardiogenic pulmonary edema B-lines are 20 expected to be bilateral, diffuse, homogeneous, and more severe in dependent areas. In ARDS 21

(and COVID-19 pneumonia) the distribution is typically patchy and heterogeneous, with abrupt 22

alternations between intense B-lines and spared areas. Anecdotally, with chronic conditions 23 such as interstitial lung diseases or lymphangitic carcinomatosis there is typically a mismatch 24

between the severity of B-line distribution and relatively milder symptoms. In bacterial 25 infection, lung contusion, and lung infarction the distribution is typically focal, and the severity 26 of the clinical condition may be disproportionate in comparison with the relatively unimpressive 27 B-line pattern. 28 29 3) Is there alveolar consolidation, and if so, what is its distribution? 30 As with B-lines, there are many potential etiologies when consolidation is detected with LUS. 31 The degree and location of consolidated lung, as well as the presence or absence of air 32 bronchograms, may suggest a particular diagnosis such as pneumonia or atelectasis (see Video  33 3). 34 35 In particular, the relationship between the area of consolidated lung and an adjacent pleural 36 effusion may be crucial to establishing a diagnosis. Compressive atelectasis (as opposed to 37 atelectasis caused by an obstructed airway, for example) is typically accompanied (and caused) 38 by a large pleural effusion, and therefore the absence of such an effusion makes this diagnosis 39

unlikely. The amount of atelectasis can also be seen to lessen with inspiration, while such 40 dynamic respiratory recruitment is usually absent in pulmonary infection or malignancy. Air 41 bronchograms, which typically move with the respiratory cycle and therefore demonstrate the 42 patency of the bronchial tree, are common in pneumonia but absent in atelectasis, particularly 43 obstructive atelectasis. 44 45

Finally, extensive consolidated areas in ARDS may respond well to recruitment maneuvers, and a 46 pattern of infero-posterior consolidation in particular may predict a positive response to prone 47 positioning [25] . The effect of recruitment maneuvers can be followed in real time using lung 1 ultrasound (see Video 3).  2  3 4) Is there a pleural effusion? 4 LUS can be used to determine the size of a pleural effusion (see Video 4) in addition to its 5 distribution, complexity, and echogenicity [34] , being careful to distinguish rib shadows from 6 pleural fluid. Thoracentesis with ultrasound guidance can be performed with low complication 7 rates, especially in mechanically ventilated patients [35] . Pleural effusion can be difficult to 8 distinguish from consolidation on CXR, and LUS is the ideal tool to make this distinction. 9 10

At this point the answers to the above-mentioned four questions can be integrated, and any 11 abnormal findings may have already led to a presumptive diagnosis. A perfectly normal LUS 12 exam, however, is also very useful. Ruling out pneumothorax, pulmonary edema, consolidation, 13 and pleural effusion in a patient with significant dyspnea or hypoxemia can lead to the 14 consideration of conditions such as pulmonary embolism, asthma exacerbation, or COPD 15 exacerbation. 16 17 5) Can I monitor changes in lung aeration? 18 While the routine application of recruitment maneuvers in ARDS remains controversial, LUS is 19 effective in monitoring lung recruitment in critically ill patients who are mechanically ventilated; 20 this potential has been demonstrated in both ventilator associated pneumonia and in ARDS [36] 21 [37] . A LUS score of both aeration and recruitment, based on the evaluation of three basic 22 patterns in 12 anterior, lateral and posterior chest areas, has been validated in comparison to 23 the pressure-volume curve in ventilated patients. Dynamic changes can be followed over time in 24 response to drugs, ventilatory strategies, and recruitment maneuvers by assigning a recruitment 25 score (positive or negative) to each lung region. 26 27 LUS is also useful in the quantification of extravascular lung water (EVLW), and compares well to 28 more invasive estimates [38] [39] [40] . This technique can be helpful in decision making around 29 fluid management in complex patients. 30 31 32 Conclusion 33

Lung ultrasound, an imaging modality quickly performed, interpreted, and integrated by the treating 34 physician at the bedside, is a particularly useful tool for acutely ill patients. Commonly encountered 35 conditions such as pneumonia, pulmonary edema, and pneumothorax can be efficiently evaluated, and 36 the skill set is generally straightforward to learn. 37 38 39 

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Study Group on Lung Ultrasound from the Molinette and Careggi Hospitals (2019) Lung ultrasound integrated with clinical assessment for the diagnosis of acute decompensated heart failure in the emergency department: a randomized controlled trial

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The "Lung Point": An Ultrasound Sign Specific to Pneumothorax

Semi-quantification of Pneumothorax Volume by Lung Ultrasound

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Safety of ultrasound-guided thoracentesis in patients receiving mechanical ventilation

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Bedside Ultrasound Assessment of Positive End-Expiratory Pressure-Induced Lung Recruitment

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Lung Ultrasound Predicts Well Extravascular Lung Water but Is of Limited Usefulness in the Prediction of Wedge Pressure

A simplified lung ultrasound approach to detect increased extravascular lung water in critically ill patients