Role of ultrasonography in the diagnosis of pleural effusion

Background Transthoracic ultrasonography (TUS) represents a useful diagnostic tool in the management of pleural diseases. It is the best method for guiding interventional procedures in the pleural space. Objectives The aim of this study was to detect the role of ultrasonography (US) in the diagnosis and management of pleural effusion in comparison with computed tomography (CT). Patients and methods Patients with suspected clinical and radiological evidence of pleural effusion were included. Routine laboratory investigations, chest radiography, CT of the chest, TUS, and thoracentesis with biochemical, bacteriological, and cytological examination of pleural fluid were carried out for all patients, and medical thoracoscopy and US-assisted interventions were carried out whenever needed. Results Eighty-four patients were included in the study. Male patients represented 56% (47 cases), whereas female patients constituted 44% (37 cases); their mean age was 51.21±14.1 years (range: 14–80 years). Seventy-three (86.9%) cases had exudative effusions; inflammatory causes (n=33) and malignancy (n=31) were the most common. TUS was equal to CT in the detection of pleural effusion, pleural thickening, hydropneumothorax, pleural nodule, and consolidation. Moreover, US was better than chest radiography in the detection of pleural thickening, encysted pleural effusion, pleural mass, and consolidation. US was better than CT in the detection of septations (n=30 vs. 5). However, CT was better than US in the detection of loculation (n=28 vs. 17) and pulmonary mass (n=8 vs. 4). Thorcoscopy was performed for nine patients, and was better than US and CT in the detection of pleural nodules. Conclusion TUS is an efficient, quick, inexpensive, radiation-free method for the evaluation of pleural diseases.


Introduction
Pleural effusion is a common medical problem; the presence of pleural effusion may be primary manifestation or a secondary complication of many disorders. As the differential diagnosis is wide, a systematic approach to investigation is necessary [1].
Imaging of the pleura can be challenging and it plays an important role in the diagnosis and subsequent management of patients with pleural disease. The presence of a pleural abnormality is usually suggested following a routine chest radiography (CXR); however, it often fails in determining the presence of locutions or septations within the effusion or in the detection of pleural thickening and fibrosis [2].
Computed tomography (CT) may show abnormalities of the pleura at an earlier stage than do other imaging techniques. It is also useful in the distinction of pleural from parenchymal lung disease, in determining the precise location and extent of pleural disease, and in certain instances it permits the characterization of tissue density within a lesion by means of analysis of attenuation coefficients [3].
As an imaging modality, transthoracic ultrasound (TUS) has many advantages, the most significant being its immediate application at the point of care and its ability to augment the clinical assessment of the respiratory system. It is relatively cheap, mobile, utilizes no radiation, and has a short examination time [4].
US can be used to clarify the nature of pleural densities, pleural effusions, and pleural thickening. It can also differentiate pleural from parenchymal lesions, visualize ill parenchyma obscured by pleural effusion and detect pleural septations and other pleural abnormalities. It aids in the differential diagnosis of pulmonary parenchymal diseases such as consolidation, atelectasis, and tumor and clarifies subpulmonary or subphrenic fluid cases and chest wall tumor mass. It allows the detection of small amounts of pleural locular fluid; US allows an easy differentiation of pleural locular liquid and thickened pleura. It is efficient in pinpointing thoracocentesis, even in small fluid collections [5]. US guidance improves the success rate of pleural aspirations, which may be as high as 97% [6].
TUS is an extremely helpful guide for biopsies of the pleura [7]. Focal pleural abnormalities can be identified with US, and biopsies can be aimed at areas of interest. Recent studies have proposed that image-guidance may significantly increase the yield while decreasing the risk for complications [8].
The aim of this work was to detect the role of US in the diagnosis and management of pleural effusion in comparison with CT. intercostally with perpendicular orientation. The patient's arms were raised and crossed behind the head to extend the intercostal spaces and facilitate access. The probe was placed in different positions to provide a three-dimensional image. Abdominal approach was adopted; the diaphragm shows a bright, curving echogenic line that moves with respiration. The lung above the diaphragm is filled with air. The curved surface of the diaphragm-lung interface acts as a specular reflector and produces a mirror image of the liver or spleen above the diaphragm. The US hallmark of pleural fluid is an echo-free zone between the parietal and visceral pleura. US images were collected for each patient.

Patients and methods
Chest US fulfilled the following points pleura was considered thickened if its thickness was more than 3 mm. (f) Assesses the invasion of tumors to the pleura and chest wall. (g) Recognizes hydropneumothorax: Hydropneumothorax is identified by placing the probe in a single site on both sides of the upper chest where air is collected due to gravity. Once visualized the parietal pleura as an echogenic horizontal line below the ribs, movement of the pleural line synchronous with respiration the 'lung sliding' and some echogenic vertical artifacts the 'B lines' their visualization immediately rules out pneumothorax while presence of horizontal artifact the 'A lines' in absence of the 'B lines' confirms presence of pneumothorax. 'Lung point' sign was considered whenever possible, which consists of alternating lung sliding and abolished lung sliding at the same spot. (8) Ultrasound-assisted interventions whenever needed (a) Diagnostic thoracentesis: An US scan was performed to confirm the presence of fluid and to select and mark the best puncture site. The sample was sent for chemical, bacteriological, and cytological examination. Each effusion was defined as transudate, an exudate, or an empyema on the basis of the level of LDH and total protein in the effusion, and the results of cytological and bacteriological examination were defined following Light's criteria [10]. (b) Pleural biopsy of pleural thickening or pleural tumor: An US scan was performed to confirm the presence of pleural thickening or mass and to select the best puncture site. The puncture was then made using real time scanning while visualizing the needle during penetration or after choosing the punctured site with US; the probe was then removed and the puncture made with careful attention paid to the depth of the collection and the localization and depth of the lung. The procedure was performed under local anesthesia using an injection of 10 cm lidocaine 2% intradermally and subcutaneously and along the needle track. Either fine needle aspiration using 16-20 G needle attached to syringe was performed for pleural mass or the biopsy was performed using Abrams pleural biopsy needle for pleural thickening. An effusion was defined as malignant if cytological examination of the fluid shows malignant cells and histological examination of the specimens obtained from pleural biopsy or Transthoracic needle aspiration biopsy showed evidence of malignant neoplasm. (c) Catheter drainage of pleural collections: External drainage of infected pleural fluid collection through a catheter inserted with US guidance (Biometrix hemodialysis latex free catheter; Biometrix, The Netherlands) is indicated in patients with a short duration of symptoms, free-flowing or unilocular effusions, absence of thick pleural peel on CT scans and fluid that can be aspirated easily with a needle [11].
(d) Medical thorcoscopy and thoracoscopic pleural biopsy: Thoracoscopic pleural biopsy was performed with a rigid thoracoscope (Karl Storz, Berlin, Germany) and this was performed to selected cases of high suspicion of malignancy, to achieve proper visualization of the pleura when taking the biopsy. US was used to localize the portal of entry to avoid complications and to give the best results of pleural visualization.

Statistical analysis
Statistical analysis was performed and statistical presentation was made using the mean, SD, and χ 2 by statistical package for social science (SPSS) 17; nonparametric data were expressed as number and percentage of the total.

Results
The present study included 84 patients with pleural effusion. There were 47 male patients and 37 female patients; their ages ranged between 14 and 80 years.
The etiology of pleural effusion and the final diagnosis were reached through combined diagnostic approach, including history, general and local examination, radiological examination, TUS finding, pleural fluid analysis (chemical, bacteriological, and cytological  (Tables 4-6 and  Figs 1 and 2).
From this study, the results showed that TUS and CT for the chest had the same sensitivity and specificity in the detection of pleural thickening with an accuracy of 97.62 (Table 7).
However, CT was better compared with US in the detection of pulmonary mass with a sensitivity, specificity, and accuracy of 100% (Table 8).
On comparison between US and CT in the detection of pleural mass, both US and CT had the same sensitivity and specificity in the detection of pleural mass with an accuracy of 97.62 (Table 9). Table 10 demonstrates that thorcoscopy is better compared with US and CT in the detection of pleural nodule.

Case 1
An 18-year-old female patient presented with dyspnea on exertion, intermittent fever, and weight   Distribution of cases according to types of pleural and pulmonary lesions detected using ultrasound versus chest radiography findings loss. Plain CXR was obtained and showed rightsided massive pleural effusion (Fig. 3a). CT scan was performed and showed marked pleural effusion in the right side with underlying lung collapse and pleural thickening (Fig. 3b and c). US showed complex septated pleural effusion. US-guided thoracocentesis was performed with analysis of fluid, which showed exudative fluid with high LDH. US-guided pleural biopsy (Abrams) was performed and it showed caseating tuberculous pleurisy (Fig. 3d).

Case 2
A 70-year-old male patient who was a farmer and a heavy smoker presented with gradual onset of progressive dyspnea, fever, and left-sided chest pain. CXR was performed and it showed massive left-sided pleural effusion (Fig. 4a). CT was performed and it showed left-sided massive pleural effusion with left lung collapse and mild right-sided pleural effusion (Fig. 4b and c). US showed complex septated pleural effusion with pleural mass on diaphragmatic pleura (Fig. 4d and e). USguided thoracentesis was performed with analysis of fluid; it showed exudative fluid with high LDH. Thoracoscopy was performed and it showed septation and pleural nodules (Fig. 4f); thoracoscopic pleural biopsy proved dysplastic mesothelioma.

Discussion
US is a useful tool for physicians managing pleural diseases. It permits imaging of pleural effusion and other pleural pathology. It can be used to clarify the nature of pleural densities, pleural effusions, and pleural thickening. It can also differentiate pleural Table 7 Comparison between ultrasound and computed tomography in the detection of pleural thickening  Distribution of cases according to types of pleural and pulmonary lesions detected using ultrasound versus computed tomography findings   from parenchymal lesions, which may be difficult in the ordinary CXR.
In the present study US demonstrated significant detection of pleural effusion in 100% (n=84) of cases, which is greater than that for CXR at 95.2% (n=80). Similar results were reported by Zanobetti et al. [12], who studied the possibility of replacing standard chest radiography with chest US for the evaluation of acute dyspnea; US detected 87 cases, whereas CXR detected 76 cases. Kalokairinou-Motogna et al. [13] also reported that US showed significantly greater detection of pleural effusion compared with radiography.
Many studies were conducted to detect the role of US in the detection of pleural diseases in comparison with radiography.
Bediwy et al. [14] reported that US had detected 70% of cases with pleural thickening, whereas CXR had    detected only 10%. Another study by Helala et al. [15] reported that US had better accuracy compared with CXR in detecting pleural thickening. These results are in agreement with the current study in which the US demonstrated a statistically significant difference compared with radiography in the detection of pleural thickening; US detected 100% of cases with pleural thickening detected by means of CT (n=26), whereas CXR did not detect any case.
Moreover, the current study demonstrated that US had a statistically significant difference compared with radiography in the detection of pleural masses and was equal in sensitivity to CT, as US and CT detected 75% of cases with pleural masses detected by means of medical thoracoscopy (6/8), whereas CXR could not detect any case.
In the present study we compared US and CT in the detection of pleural lesions and found that US is better than CT in the detection of pleural effusion, as US detected all (84/84) cases of effusion, even the small subpulmonic effusion, whereas CT detected 98.8% (83/84) of cases and missed one case.
This is in agreement with the results of Helala et al. [15], who reported that US (49/50) was better compared with CT (45/50) in the detection of pleural effusion in critically ill ICU patients. Moreover, these results are in agreement with the study by Abu-Youssef et al. [16], who reported that US and CT were well correlated in the detection of pleural effusion and there was no statistically significant difference between US (100%) (n=16) and CT (100%) (n=16) in the detection of pleural effusion.
In the current study, CT demonstrated a statistically significant difference compared with US in the detection of encysted effusion, as CT detected 100% (n=28) and US detected 60.7% (n=17). In agreement with our results, Kurian et al. [17] reported that 100% (n=15) effusions were encysted on chest CT, and 86.6% (n=13) were encysted on TUS on comparing US and CT in the evaluation of pneumonia complicated by parapneumonic effusion in children. However, in disagreement with these results, Abu-Youssef et al. [16] reported that US was superior to CT in the detection of encysted effusion, as US detected 11/11 cases with encysted pleural effusion, whereas CT detected only 4/11 cases with encysted pleural effusion. This may be attributed to their definition of encysted effusion, as they considered every fluid with septations seen on US as encysted effusion.
In the current study, nine patients were subjected to medical thoracoscopy, and thoracoscopy was better compared with US and CT in the detection of pleural nodules with a statistically significant difference (Table 10). In disagreement with our results, Khalil et al. [18] reported that diaphragmatic and costal nodules were found on medical thorcoscopy in all cases reported on US. However, thoracoscopy was better than US in the detection of septations and pleural thickening, but with no statically significant difference. In agreement with our results, Khalil et al. [18] reported three relevant false-negative results as US missed thick septations in a morbidly obese patient with degraded US images.
In the present study, chest radiographs were a nonsensitive imaging technique for diagnosing pleural thickening, pleural nodules, and plural masses. The results are in agreement with those of Müller [19], who reported that chest radiography is of limited utility and is nonsensitive in demonstrating plural opacity.
This study has some limitations: small number of cases included in this study is the most important one. Moreover, the number of diagnostic interventions in this study cannot give an idea about the diagnostic yield and complications. Therefore, wider range studies of interventions and US-guided interventions (diagnostic and therapeutic) should be encouraged.

Conclusion
TUS is a safer alternative to radiology (radiography or CT) for the diagnosis of pleural lesions but with less diagnostic value for pulmonary diseases. Chest US provides much useful diagnostic information, including detection of a small volume of pleural fluid; it is also a useful tool to guide percutaneous transthoracic aspiration biopsy of pleural lesions.

Financial support and sponsorship
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Conflicts of interest
There are no conflicts of interest.