Role of chest ultrasonography in differentiating between acute cardiogenic pulmonary edema and acute respiratory distress syndrome

Introduction Sometimes it is difficult to differentiate between acute cardiogenic pulmonary edema (APE) and acute respiratory distress syndrome (ARDS) on clinical basis only. Chest ultrasonography (CUS) may be helpful in providing ultrasonographic pleuropulmonary signs, which aids in such differentiation. Aim The aim of this study was to evaluate the role of CUS in differentiating between ARDS and APE through the characterization of comparative peculiar ultrasonographic pleuropulmonary signs. Patients and methods On admission, CUS was performed in Ain Shams University Hospital and Al-Abbassia Chest Hospital ICUs on 28 consecutive patients who presented with ARDS (15 cases) or APE (13 cases). CUS examination focused on the detection of the following pleuropulmonary signs in both ARDS and APE: alveolar–interstitial syndrome (AIS), pleural line abnormalities, absent or reduced lung sliding, consolidation, and pleural effusion. Results AIS was found in 100% of patients with ARDS and in 100% of patients with APE. Pleural line abnormalities were observed in 100% of patients with ARDS and in 0% of patients with APE (P=0.001). Absent or reduced lung sliding was observed in 100% of patients with ARDS and in 0% of patients with APE (P=0.001). Consolidations were present in 93.3% of patients with ARDS in 7.5% of patients with APE (P=0.001). Pleural effusion was present in 40% of patients with ARDS and in 76.9% of patients with APE (P=0.049). All pleuropulmonary signs, except the presence of AIS, presented a statistically significant difference in presentation between ARDS and APE, resulting peculiar ultrasonographic pleuropulmonary signs of ARDS. Conclusion CUS represents a useful tool for differentiating ARDS from APE in ICU patients. In fact, the presence of absent or reduced lung sliding, pleural line abnormalities, and lung consolidations on a background of AIS seems diagnostic of ARDS.


Introduction
Rapid and accurate identification of thoracic emergencies may be a challenging task to pulmonary critically ill physicians. Traditionally, relying on historical and physical examination findings in the preliminary differential diagnosis of acute respiratory distress may be unreliable. Thus, sometimes it is difficult to differentiate between acute cardiogenic pulmonary edema (APE) and acute respiratory distress syndrome (ARDS) [1][2][3].
A new definition of ARDS, the Berlin definition, has been published. ARDS is an acute diffuse, inflammatory lung injury, leading to increased pulmonary vascular permeability, increased lung weight, and loss of aerated lung tissue with hypoxemia and bilateral radiographic opacities, associated with increased venous admixture, increased physiological dead space, and decreased lung compliance [4].
Chest ultrasonography (CUS) is increasingly used in the management of ICU patients [5,6]. CUS has a higher diagnostic accuracy for pleural effusion, consolidation, and interstitial syndrome when compared with bedside chest radiography in patients with ARDS [7]. Different studies have addressed the ultrasonographic appearance of ARDS, but few studies have been able to give a detailed characterization of the syndrome, permitting a differential diagnosis from the ultrasonographic appearance of APE [2].
This study aimed to evaluate the role of CUS in differentiating between ARDS and APE through the characterization of comparative peculiar ultrasonographic pleuropulmonary signs.

Patients and methods
This prospective study was conducted in the Respiratory ICU of Ain Shams University Hospital and Al-Abbassia Chest Hospital during the period between December 2013 and December 2014 and consecutive patients admitted and fulfilling Berlin ARDS definition and diagnostic criteria of ARDS were recruited [4]. In addition, patients consecutively admitted with the diagnosis of APE on the basis of clinical signs and symptoms, ECG, chest radiography, and echocardiography (not in all cases) were also included in the study.
As CUS is now part of routine diagnostic procedures in our unit, no informed consent or approval of ethics committee was requested.
All patients underwent CUS on the first day of admission and after being diagnosed based on clinical and radiological data. A convex (curvilinear) probe operates at a frequency between 2 and 8 MHz and a linear probe operates at a frequency of 5-10 MHz [Sonoline G20 Ultrasound Imaging System (Siemens, Mountain View, California, USA) at Al-Abbassia Chest Hospital and Mindray M5 (Mindray M5Bio-Medical Electronics Co., Shenzhen, China) at Respiratory ICU, Ain Shams University Hospital] were used for lung examination.
The examination was performed at patient bedside. Lateral or seated positions were used to scan the posterior thorax. In patients in whom the seated position was not possible, a lateral decubitus position was used to examine posterior lung regions [2]. Probes were placed horizontally and/or vertically along each intercostal space (the parasternal line, anterior axillary line, and posterior axillary line) on both sides. Data were displayed on a screen. Each hemithorax should be divided into five zones: two anterior zones separated by the third intercostal space, two lateral zones, and one posterior zone [8].
For each echographic acquisition, we investigated the following four ultrasonographic markers: (1) Lung gliding or sliding was defined as evidence of pleural movement; lung gliding presence indicates a pulmonary region in contact with the thoracic wall and excludes pneumothorax [9]. (2) A lines, defined as horizontal reverberation (transduce reverberation), reflect the pleural line in depth; the presence of A lines is a normal finding [9]. (3) Ultrasound lung comets or B lines, defined as ring down, vertical reverberation, extend to the inferior margin of the screen, masking A lines. They define interstitial syndrome (pulmonary edema and interstitial disease) [9]. (4) Alveolar syndrome, defined as organization (hepatization) of the pulmonary field with a solid appearance, can sometimes show evidence of aerated bronchi (air bronchogram), which, when present, indicates a consolidation or a partially aerated alveolar syndrome [10].
Chest ultrasonography pleuropulmonary finding characteristics (1) Alveolar-interstitial syndrome (AIS) is defined as the presence of more than three ultrasound lung comet means (B lines) or 'white lung' appearance for each examined area [2]. (2) Pleural line abnormalities are defined as thickenings greater than 2 mm, evidence of small subpleural consolidations, or coarse appearance of the pleural line; its presence means that a process, either consolidations or inflammatory process, is present as in cases of ARDS, and its absence means acute process is present as in APE limited by diaphragm and the costal pleura [10].

Statistical analysis
The collected data were revised, coded, tabulated, and introduced into a PC using statistical package for the social sciences (SPSS 15.0.1 for Windows, 2001; SPSS Inc., Chicago, Illinois, USA). Descriptive statistics was performed and parametric numerical data were presented as mean±SD and range, whereas as median and interquartile range for nonparametric numerical data. Non-numerical data were presented as frequency and percentage. Analytical statistics was performed and Student's t-test was used to assess the statistical significance of the difference between two study group means. The χ 2 -test was used to examine the relationship between two qualitative variables. Fisher's exact test was used to examine the relationship between two qualitative variables when the expected count is less than 5 in more than 20% of cells. A P value of more than 0.05 was considered as nonsignificant, P value of less than 0.05 as significant, and P value of less than 0.01 as highly significant.

Results
The study included 28 patients. Fifteen met the criteria for the diagnosis of ARDS and 13 had APE.
There were 13 (46%) male and 15 (54%) female patients. The demographic characteristics of studied patients are shown in Table 1.
Comparison between ARDS and APE cases as regards ultrasonographic findings are shown in Table 2. AIS was present in all of our study populations (ARDS and APE), indicating its high sensitivity in the diagnosis of increased extravascular lung water. AIS of ARDS appear dyshomogeneous, whereas that of APE appears homogeneous. All other ultrasonography signs presented a statistically significant difference in presentation between the two groups. The sensitivity and specificity of each ultrasonographic sign in ARDS and APE, respectively, are illustrated in Tables 3 and 4.

Discussion
This study demonstrated the ability of CUS in the identification of characteristic pleuropulmonary signs useful in the diagnosis of ARDS and APE. The presence of ultrasonographic pleuropulmonary signs of dyshomogeneous AIS, such as absent or reduced lung sliding, pleural line abnormalities, and lung consolidations, is strongly predictive of ARDS diagnosis.
Standard chest radiograph is still performed in the assessment of patients presenting with ARDS. Chest radiograph interpretation is unreliable and compares poorly with computed tomography (CT) scanning in patients with ARDS [4,11]. Chest CT scanning use has led to a better understanding, diagnosis, and management of ARDS. CT scanning allows understanding that alveolar filling, consolidation, and atelectasis occur predominantly in dependent lung zones, whereas other areas may be relatively spared with nonuniformity of degree of lung injury severity in different lung areas [12,13]. CT scanning has disadvantages in ARDS assessment, such as the high dose of radiation exposure to the patient, being expensive, the need to move the patient into the radiology room, and the lack of CT scanning in some hospitals [14].
The benefits of ultrasonography use in pulmonary critically ill patients is that it is rapid, noninvasive, inexpensive, portable, and nonirradiating tool. CUS became a very important diagnostic tool nowadays [15].   As regards ARDS, it is sometimes difficult to be differentiated from APE. This study searched for characteristic ultrasonographic pleuropulmonary signs helpful in the differentiation between ARDS and APE.
It has been previously stated that ultrasonographic signs of AIS is a marker of pulmonary edema being present both in acute lung injury (ALI) or ARDS and APE patients [8].
In the present study, both ARDS and APE patients had AIS, which is diffuse B-line profile. This is in agreement with the study by Copetti et al.
[2] on 58 patients fulfilling criteria for either ALI/ARDS (18 cases) or APE (40 cases), which revealed diffuse B lines in all patients (2). Similar findings were reported by Zanobetti et al.
[3], who studied 404 patients presented to the ED with dyspnea independently from the underlying disease. They compared CUS findings in some diseases in relation to chest radiography. They found that the presence of diffuse B-line profile was the characteristic ultrasonographic pattern of diffuse AIS, which is often a sign of APE. Moreover, this is in agreement with study by Daabis et al. [16], who studied 100 ICU patients presenting with acute respiratory failure. ARDS was present in 10 cases. They compared CUS with current diagnostic tools for diagnosing the etiology of acute respiratory failure. They found characteristic ultrasound B profile in all of the ARDS cases [16].
In the current study, characteristic ultrasonographic signs of consolidation were found in 53.6% of cases, which was nearly comparable to that reported by Zanobetti et al.
[3], who found that consolidation was found in 60% of cases. On comparing between noncardiogenic (ARDS) and cardiogenic (APE) origin of consolidation, the present study found that consolidation was seen in 93.3% of ARDS and never seen in APE (0%). This correlated with the study by Copetti et al.
[2], who found that lung consolidation was seen in 83.3% of cases of ARDS in comparison with 0% of cases of APE. Arrows show Pleural line abnormalities.

Figure 4
Arrow indicates Lung consolidation with air bronchogram in ARDS.   On the basis of the sensitivity and specificity of ultrasonographic pleuropulmonary signs detected in ARDS patient, peculiar findings for ARDS is reached. In case of AIS, the presence of absent or reduced lung sliding, pleural line abnormalities, and lung consolidations is strongly predictive of ARDS.
Small sample size, lack of echocardiography validation in all cases for APE diagnosis, and lack of CT scanning for verification of findings are the apparent limitations for current study.
Future studies comparing CUS-specific ultrasonographic findings with CT are needed to validate our results. This validation may limit CT use in ICU.

Conclusion
Our results demonstrate that CUS represents a useful tool for differentiating ARDS from APE in critically ill ICU patients. In fact, the presence of absent or reduced lung sliding, pleural line abnormalities, and lung consolidations on a background of AIS seems diagnostic of ARDS.

Financial support and sponsorship
Nil.

Conflicts of interest
There are no conflicts of interest.