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Original Research

Accuracy of Bedside Lung Ultrasound as a Rapid Triage Tool for Suspected Covid-19 Cases

Karagöz, Arif MD; Sağlam, Caner MD; Demirbaş, Hakan Bariş MD; Korkut, Semih MD; Ünlüer, Erden Erol MD; Prof

Author Information
doi: 10.1097/RUQ.0000000000000530

Abstract

The novel coronavirus disease 2019 (Covid-19) outbreak began in Wuhan, China, in December 2019.1 Since then, the disease has spread nearly all over the world. There are more than 7 million confirmed cases and 418,000 deaths caused by Covid-19.2 This rapidly spreading disease caused an urgent health care problem, even in developed countries. Today, strategies are focused on efforts to reduce the incidence, morbidity, and mortality of Covid-19. The emergency department (ED) is on the frontline in this struggle against Covid-19. Emergency physicians (EPs) need new resources and tools to correctly triage patients and identify those with a high risk of progression of the disease.

The most common symptoms of Covid-19 are fever and cough. The median incubation period is 4 days.1 The characteristic of the disease is development of a pneumonia that causes ground-glass opacities on chest computed tomography (CT) (Fig. 1). Another characteristic finding for laboratory testing is lymphocytopenia, and it is seen in 83.2% of patients on admission.3 The shortage of highly sensitive reverse transcriptase polymerase chain reaction tests for the diagnosis of Covid-19 has led many in the health care community to consider a screening or diagnostic role for imaging modalities.4 Publications from China during the outbreak there suggest a central role for CT, and patients were diagnosed mainly with CT.4 Ionizing radiation exposure from these CT scans poses an additional cancer risk in patients, especially younger ones.5 Transferring patients suspected of having Covid-19 to CT has the risk of spreading the infection to the other parts of the hospital, and it also poses a risk to other patients using the CT facility. So, evaluating patients in the triage area for suspicion of Covid-19 with an effective and harmless tool is very important.

FIGURE 1
FIGURE 1:
Three chest CT images of different patients depicting multifocal ground-glass appearance typical for Covid-19 pneumonia. (A) A 73-year-old male patient, (B) a 66-year-old male patient, and (C) a 38-year-old female patient.

Bedside ultrasound (BUS) is an effective tool for physicians and other health care professionals in different clinical areas.6 It is cheap, readily available, repeatable, easy to learn and perform, and does not pose any risk, with its harmless nature.7 Bedside lung ultrasound (BLUS) is more sensitive and specific than chest X-ray, and its sensitivity and specificity is near that of CT for many lung pathologies.8,9 Emergency departments are one of the places that BUS has been used for different clinical scenarios.10–14 The existing BLUS workforce can easily be upskilled for patients with Covid-19.15

We aimed to investigate the accuracy of BLUS for diagnosing pneumonia caused by Covid-19, and its effectiveness for the correct triage of patients with suspected Covid-19. With a suitable scientific result, BLUS can be the best imaging method for Covid-19 pneumonia, especially in a pandemic, such as what the world is experiencing nowadays.

MATERIALS AND METHODS

This study was a prospective, cross-sectional cohort study that was conducted April 1 to 15, 2020, at an academic, adult tertiary care center ED of a research and training hospital in Turkey. The Turkish Ministry of Health and the local ethics committee approved the study protocol. Written informed consent was obtained from each patient before their sonographic examinations.

All ED patients who were admitted with the complaint of fever, cough, and dyspnea were accepted as suspected Covid-19–related symptoms. During their working shifts, for this study, 3 European Accreditation Council certified EPs with at least 5 years of experience in BUS screened the patients who were suspected of having Covid-19. Bedside lung ultrasound was performed in the Covid-19 triage area of our ED at the time of presentation before performing other diagnostic tests. The triage physicians were not informed of the results of the BLUS, as to prevent any potential morbidity from the use of a misinterpreted examination. Patients were ineligible if they were younger than 18 years, had acute chest pain, were pregnant, were hypotensive (systolic blood pressure, <90 mm Hg), had previous thoracic surgery, were admitted when the EPs who performed BLUS were not on the shift, or if they could not get the optimal image because of technical limitations. We had recruited 72 patients by the end of the study period that was approved by the ethical committee. Before the study, 3 EPs had 3 hours of theoretical training, as well as hands-on training with 20 patients, led by an experienced radiologist to refresh their knowledge about the BLUE protocol. We did not statistically investigate the interrater agreement between sonographers to avoid any patient-to-patient and also patient-to-physician contamination.

Of those patients who granted consent to be included in the study, the EPs performed the BLUS on the supine patient using a HD11XE model ultrasound machine with a 3.6-MHz microconvex transducer (Philips Ultrasound System, Andover, MA); ultrasonographic views were recorded blindly by the EPs. This procedure took less than 2 minutes. An evaluation form was completed by each EP. Formal official CT reports of the patients were accepted as the criterion standard in our study.

The BLUE protocol, which is an internationally accepted method for BLUS and is based on careful analysis of lung ultrasound, was developed by Lichtenstein and Mezière.16 According to this protocol, as the first step, the performer evaluates the chest anteriorly and posteriorly, which are called the BLUE points.17 Specifically designed for the BLUE protocol, the BLUE points make lung ultrasound simple. They are standardized and therefore reproducible, associating clinical efficiency and ease of use. The normal artifact is the repetition of the pleural line, a roughly horizontal hyperechoic line parallel to the pleural line. We called this artifact the A line. Air blocks the ultrasound beam, which comes back to the central unit, yielding this regular artifact. The distance between the pleural line and A line is equal to the skin-pleural line distance. The other main artifact is the vertical B line.17 In the case of lung consolidation, we have 3 different pathological image options with ultrasound scanning: (1) localized appearance of the B lines (more than 3 in 1 image area), (2) hepatization sign (occurrence of liver-like echogenicity with hyperechoic air filled bronchograms), or (3) shred sign (loss of smooth continuous and even surface of the pleural line) (Fig. 2, Videos 1–3, http://links.lww.com/RUQ/A230, http://links.lww.com/RUQ/A231, http://links.lww.com/RUQ/A232).17,18 Based on these diagnostic findings on lung ultrasound, the EPs performed BLUS on the supine patient. Sterile adhesive stretch film was applied to the ultrasound probe before scanning to avoid contamination. Extra care was taken to keep the device clean and sterile as much as possible. The formal final official radiology reports of the CTs were reviewed. Sonographer EPs and radiologists were blind to each other.

FIGURE 2
FIGURE 2:
(A) Focal multiple (more than 7), coalescent B lines on ultrasound scan which is correlate with computerized tomography ground glass areas (arrow). (B) Ultrasound image depicting uneven fractal pleural border (shred sign) (arrow 1) and focal B lines (arrow 2). (C) Another ultrasound image depicting shred sign (arrow).

Statistical Analysis

A preliminary analysis was performed using the point prevalence survey. The point prevalence of Covid-19 cases in triage was calculated as 30% before the study. The sample size was conducted with the references of Buderer.19 We assumed that the prevalence of the disease was 30%, with both a sensitivity and specificity of 95%, respectively, and a dropout rate of 10%. We have calculated the corrected sample size to be 68. Normality analysis of continuous measures was performed using Kolmogorov-Smirnov analysis, Shapiro-Wilk test, and Q-Q plots. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of BLUS were calculated and analyzed using MedCalc statistical software (MedCalc Software Ltd., Ostend, Belgium). Continuous variables are reported as the means with standard errors and 95% confidence intervals (CIs) when it is needed. The maximum type 1 error was 0.05 in this study, and the level of significance was accepted as a P value less than 0.05.

RESULTS

During the study, 85 patients were admitted to the Covid-19 triage area of our ED when the 3 sonographer EPs were on their shifts and underwent screening. The number that was excluded amounted to 13, of which 3 had malignancies, 7 refused to give informed consent, and 3 had poor image acquisition. A total of 72 patients were included in the study. The diagram for the study is depicted in Figure 3.

FIGURE 3
FIGURE 3:
Study flow diagram.

The mean age of study population was 51 years (range, 20–96 years). The female and male numbers were 31 (43.05%) of 72 and 41 (56.95%) of 72, respectively. In all, 32 patients had a history of chronic diseases. The most common chronic diseases were hypertension, chronic obstructive pulmonary disease, and diabetes mellitus. Table 1 shows other demographic data.

TABLE 1 - Characteristics of Study Subjects
Mean age (min-max), y 51 (20–96)
Male 41 (56.95%)
Female 31 (43.05%)
Vital signs
 Temperature, °C 37.1 (36.3–39.5)
 Respiratory rate, /min 15.9 (12–30)
 Pulse rate, /min 93.4/min (56–146)
 SpO2 level, % 95.3% (56%–99%)
 Systolic BP, mm Hg 125.4 (82–170)
 Diastolic BP, mmHg 72.3 (43–96)
Comorbidities
 Absent 40/72 (55.5%)
 Present 32/72 (44.5%)
 COPD 12/72 (16.6%)
 Hypertension 16/72 (22.2%)
 Diabetes mellitus 6/72 (8.3%)
 CAD 5/72 (6.9%)
 Others 11/72 (15.3%)
SpO2, oxygen saturation; BP, blood pressure; COPD, chronic obstructive pulmonary disease; CAD, coronary artery disease.

Bedside lung ultrasound was performed in patients presenting to the ED with suspected Covid-19 disease. Interpretation of chest CT by the radiologist was kept as a reference. Of 39 patients who had normal chest CTs, the EPs, by BLUS, evaluated the lungs as normal in 36 patients, with the 3 remaining patients considered as false positives. Of 33 patients with positive CT findings for Covid-19 pneumonia, the EPs detected ultrasonographic findings for consolidation in 32 patients, with 1 patient considered to be a false negative (Table 2). Researchers have demonstrated the detection of lung involvement for patients with Covid-19 by BLUS carrying good sensitivity and an even excellent specificity of 96.97% (95% CI, 84.24%–99.92%) and 92.31% (95% CI, 79.13%–98.38%), respectively. The PPV, NPV, positive likelihood ratio (LR), negative LR, and accuracy of the study were 84.38% (95% CI, 64.52%–94.14%), 98.61% (95% CI, 91.15%–99.80%), 12.61 (95% CI, 4.24–37.45), 0.03 (95% CI, 0.00–0.23), and 93.71% (95% CI, 85.39%–98.07%), respectively (Table 3).

TABLE 2 - Characteristics of the Test Results
Thorax CT Positive Thorax CT Negative Total
PoCUS positive 32 3 35
PoCUS negative 1 36 37
Total 33 39 72
PoCUS, point-of-care lung ultrasound.

TABLE 3 - The Performance of BLUS for Diagnosing Covid-19 Pneumonia Compared With Thorax CT
Statistic Value 95% CI
Sensitivity 96.9% 84.2–99.9%
Specificity 92.3% 79.1–98.3%
Positive LR 12.6 4.4–37.4
Negative LR 0.03 0.0–0.2
PPV 84.3% 64.5–94.1%
NPV 98.6% 91.1–99.8%
Accuracy 93.7% 85.3–98.0%

The area under curve value in receiver operating characteristic analysis, which evaluated the rate of BLUS detecting the presence or absence of Covid-19 pneumonia, was calculated to be 0.946 (95% CI, 0.866–0.986). This value was found to be statistically significant with a P value less than 0.0001 (Fig. 4).

FIGURE 4
FIGURE 4:
ROC analysis, which evaluated BLUS's rate of detecting the presence or absence of Covid-19 pneumonia. ROC, receiver operating characteristic.

DISCUSSION

Emergency physicians are widely using ultrasound to accurately diagnose many diseases and guide many procedures. There is growing evidence that support using BUS for pathologies and procedures, such as pneumonia, hemoperitoneum, appendicitis, heart failure, pneumothorax, lumbar puncture, arthrocentesis, and central venous access.6,20–22 With its noninvasive nature, lack of ionizing radiation, cost-effectiveness, and ease of use at the patient's bedside, BUS is a valuable tool, especially for EPs.23 Chest X-ray is a routine tool for detecting lung pathologies in daily routine, but its sensitivity and specificity was found to be low for pleural effusion, pneumonia and pneumothorax.24–27 Bedside lung ultrasound has been investigated for the diagnosis of pneumothorax, pleural effusions, and other thoracic conditions and has been found to be more accurate at diagnosing these pathologies than chest X-ray and even close to CT for diagnosing lung consolidation.9,28 Cortellaro et al29 studied BLUS for the diagnosis of pneumonia and compared it with CT in the ED. They found the sensitivity of BLUS to be 98%, with a specificity of 95%. Bourcier et al26 found the sensitivity of BLUS to be 95% for diagnosing pneumonia in the ED. In a recent study conducted in the ED, Sezgin et al30 found the ultrasonographic diagnosis of lung consolidation had a sensitivity of 87.8% and a specificity of 91.7% compared with CT for the diagnosis of pneumonia. Our results are consistent with the results of these studies.

Wuhan, the capital of Hubei Province in China, became the center of an outbreak of pneumonia of unknown cause in December 2019. By January 2020, Chinese scientists had isolated a novel coronavirus, 2019-nCoV, from these patients with virus-infected pneumonia, which was later designated Covid-19 by the World Health Organization.31–33 The clinical spectrum of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) infection appears to be wide, from asymptomatic infection or mild upper respiratory tract illness to severe viral pneumonia with respiratory failure and even death, with many patients being hospitalized with pneumonia in Wuhan.31,34–37 The most common symptoms of patients with Covid-19 on admission were fever and cough, followed by sputum production and fatigue.31 These are common symptoms among the patient population being admitted to EDs, too. Early recognition of the lung involvement of Covid-19 is very important, because lung involvement seems to play a critical role for the development of pneumonia, acute respiratory distress syndrome, and multiorgan failure.37,38 In a pandemic with lots of patients being admitted to EDs with respiratory symptoms, BLUS has the potential to be a very useful tool to triage patients correctly. It can allow the utilization of the correct sources for patients, as well as save time and money.

All of the 3 sonographers in our study were experienced with BLUS, and this situation lowered the number of patients excluded as a result of low image quality. Novice sonographers may have a higher rate of nondiagnostic BLUS scans, but in a normally aerated lung, the only detectable structure is the pleura, which is visualized as a hyperechoic horizontal line, and the only artifact is the A line repeated regularly, which is easy to diagnose (Fig. 5).7 They will be better at excluding the pathology and diagnosing “normal” lungs at the beginning. Because BLUS is easy to learn, they will decrease their number of nondiagnostic scans over time.7

FIGURE 5
FIGURE 5:
(A) Normal lung ultrasound image depicting clear and even pleural line and A lines repeated regularly. (B) Normal lung ultrasound image depicting clear and even pleural line and A lines with nonpathologic b lines (comet-tail artifacts) (arrow).

To the best of our knowledge, this is the first study investigating the role of BLUS for diagnosing lung involvement of Covid-19 disease. Our study has shown that BLUS can be used for the triage of patients with suspected Covid-19 in EDs. It can help to reduce the numbers of CT scans for this group of patients and protect them from radiation exposure. It allows physicians to detect all of the patients, regardless of the severity of their symptoms, with a noninvasive and harmless tool with a high rate of overall accuracy.

Limitations

The first limitation of our study is that we did not calculate the κ statistic for interrater reliability between the 3 EPs that performed the BLUSs to avoid any possible patient-to-patient contamination. Second, we have evaluated the chest CTs and BLUSs as “positive” or “negative” for lung involvement of Covid-19, but we did not evaluate the severity of the lung pathology as mild, moderate, or severe according to dissemination of the lung pathology for positive cases neither by BLUS nor by CT. A new scientific study should be conducted comparing the spread of the disease in lungs with BLUS and CT. Third, we have conducted the study with EPs in the triage area, but lots of EDs have only assistant medical staff other than the physicians at triage. As a result, it would be great to determine the ability of an assistant staff to perform BLUS on suspected Covid-19 cases to increase the applicability of BLUS in the triage area.

CONCLUSIONS

Bedside lung ultrasound can be used to detect the presence of pulmonary involvement in cases of suspected Covid-19 in the ED for the effective triage of patients. Further studies are needed.

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Keywords:

coronavirus; pneumonia; ultrasonography; point-of-care testing; emergency medicine

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