Egyptian Journal of Chest Diseases and Tuberculosis (2013) 62, 429433

The Egyptian Society of Chest Diseases and Tuberculosis

Egyptian Journal of Chest Diseases and Tuberculosis

www.elsevier.com/locate/ejcdt www.sciencedirect.com

ORIGINAL ARTICLE

Discrimination between pleural thickening and minimal pleural eusion using color Doppler chest ultrasonography
Ali A. Hasan *, Hoda A. Makhlouf, Alaa R.M. Mohamed
Chest Department, Faculty of Medicine, Assiut University, Egypt Received 10 May 2013; accepted 19 May 2013 Available online 20 June 2013

KEYWORDS Pleural effusion Ultrasound on gray scale Color Doppler ultrasound Fluid color sign

Abstract Background: The discrimination of pleural thickening from minimal pleural effusion may be difcult as both lesions appear as anechoic on grayscale ultrasound, hence, free of echoes does not conrm the presence of pleural uid. Aim of this study: To evaluate the value of color Doppler ultrasound in differentiating minimal pleural effusion that could be aspirated from pleural thickening and to compare it with grayscale ultrasound. Patients and methods: This analytic cross-sectional study was done prospectively on 40 patients who presented with pleural based opacity in their chest radiographs compatible with minimal pleural effusion. Gray scale ultrasound was done for all patients then color Doppler ultrasound examination was applied to detect the presence or absence of uid color sign. The presence or absence of pleural effusion was conrmed by aspiration of pleural uid. Results: The sensitivity of real time gray scale ultrasound in detecting minimal pleural effusion and differentiating it from pleural thickening was 95.5% while, specicity was 33%, and accuracy was 67%. The ability of ultrasound in discrimination of minimal pleural effusion from pleural thickening improved greatly by application of the color Doppler examination where the specicity of the method reached 100% while the sensitivity was 91% and accuracy was 95%.

* Corresponding author. Address: Chest Department, Faculty of Medicine, Assiut University, Assiut University Hospital, Assiut University, Assuit 71111, Egypt. Mobile: +20 1003564805; fax: +20 882333327. E-mail address: aabdelazeem@yahoo.com (A.A. Hasan). Peer review under responsibility of The Egyptian Society of Chest Diseases and Tuberculosis.

Production and hosting by Elsevier

0422-7638 2013 The Egyptian Society of Chest Diseases and Tuberculosis. Production and hosting by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ejcdt.2013.05.010

430

A.A. Hasan et al.

Conclusions: Application of color Doppler examination increases the accuracy of real time chest ultrasound to discriminate pleural thickening from minimal pleural effusion and hence color Doppler examination proved to be a useful diagnostic tool to real-time gray-scale ultrasound for diagnosis of minimal pleural effusion.
2013 The Egyptian Society of Chest Diseases and Tuberculosis. Production and hosting by Elsevier B.V. All rights reserved.

Introduction Pleural thickening and brosis may resemble pleural effusion in plain chest X-ray or even in CT chest and this may lead to invaluable trial for needle aspiration. Small amounts of pleural effusion can be detected with ultrasound. Using chest ultrasound, pleural effusion appears as an echo-free space between both parietal and visceral pleura and shape of this may be changed with respiration [1]. The discrimination of pleural thickening from minimal pleural effusion may be difcult as both lesions can appear as anechoic on grayscale ultrasound, therefore, free of echoes does not guarantee the presence of pleural uid [2,3]. As any movement of body uid may be translated into colored images, color Doppler imaging was recently used to solve this problem. It was observed that color signal may appear within the uid collection in the pleural space during respiratory and cardiac cycles (uid color sign) [4]. In case of pleural thickening no colored signals are detected as pleural thickening has no movable part [5]. This study was to evaluate the accuracy of color Doppler ultrasound in differentiating minimal pleural effusion that could be aspirated from pleural thickening and to compare it with grayscale ultrasound. Patients and methods This analytic cross- sectional study was carried out on 40 patients suspected to have minimal pleural effusion based on their chest X-ray. They were selected from those attended to the Chest Department, Assiut University Hospitals, Egypt. Informed consent was obtained from each participant and the study was approved by the Faculty of Medicine Ethical Committee. Method The followings were done for the enrolled patients: After medical history and physical examination pleural effusion was suspected rstly by the presence of blunting of lateral costophrenic angle on upright posteroanterior radiographs and blunting of the posterior costophrenic angle on lateral radiographs [1]. Gray scale ultrasound was done by an ultrasound scanner (Aloka Echo Camera SSD-3500; Aloka Prosound; Japan) equipped with a 3.5-MHz convex probe to detect the presence of pleural effusion. The scanning was done using the intercostals space as an acoustic window with the patient in a sitting or supine position rising his arms above his head to widen the intercostal space and facilitate scanning. On ultrasound gray scale pleural effusion appeared as an anechoic layer between the visceral pleura and the parietal pleura [1]. Split pleural signs, the internal echogenicity of the effusion, the change of shape during respiration, the presence of the mo-

bile septa, and thickening of the pleura and the presence of organized uid in the pleural space were analyzed. Before the start of the Color Doppler ultrasound examination, the Doppler lter is usually set at 50100 Hz to eliminate low-frequency signals from vessel wall motion and avoid interference from respiratory and cardiac movement. Color Doppler gain is also adjusted until only a few noise specks are visible in the background [68]. During scanning the patients with color Doppler, the sensitivity of the Doppler should be set to low ow or the low-velocity scale (typically 0.25 m/sec) [1]. As pleural thickening has no movable part, the colored signals will not be detected in cases of pleural thickening [5]. Finally the diagnosis of aspirable pleural effusion was followed by needle aspiration to conrm the presence of pleural uid (4). Statistical analysis Statistical analysis was performed using Statistical Package for the Social Sciences (SPSS-version 17) software. The results were expressed as mean standard deviation or frequencies. Proportions were compared with chi-square tests. The sensitivity, specicity, accuracy positive predictive value and negative predictive value were calculated as follows:
Sensitivity true positive=true positive false negative Specificity true negative=true negative false positive Accuracy true positive true negative=true positive false positive true negative false negative Positive predictive value true positive=true positive false positive Negative predictive value true negative=true negative false negative

Results Forty patients, 27 men and 13 women with mean age 43.77 16.47 were evaluated for the presence of minimal pleural effusion (Table 1). Pleural effusion was conrmed by aspiration in 22 (55%) out of 40 cases. The remaining 18 (45%) cases had pleural thickening. Real time gray scale ultrasound showed anechoic area between the visceral and parietal pleura compatible with pleural effusion in 33 (85.5%) patients from a total of 40 patients while the remaining 7 cases (15.5%) were diagnosed as pleural thickening. However, by color Doppler ultrasound pleural effusion was detected in 20 (50%) patients and pleural thickening was diagnosed in 20 (50%) patients (Table 2). Real time gray scale ultrasound detected pleural effusion in 21 patients from a total of 22 patients with conrmed pleural effusion by aspiration with a sensitivity 95.5%. However, in another 12 patients whose pleural effusion had not been conrmed; gray scale US showed pictures compatible with pleural effusion (12 false positive cases). From 18 patients without pleural effusion, gray scale ultrasound showed pleural

Color Doppler Chest Ultrasonography in diagnosing minimal pleural effusion

Table 1
Variable Age (years) Gender Male Female Data are expressed as mean SD or number (%)

431

Demographic data of the study group.

Study group (n = 40) 43.77 16.47 27 (67.5%) 13 (33.5%)

chest X-ray [9]. In addition many pleural lesions as pleural thickening and brosis may mimic minimal pleural effusion in plain radiograph. Chest ultrasonography has a well documented role in diagnosis of pleural effusion as it is primarily used to conrm the presence of effusion in a patient with abnormal chest radiographs being able to detect as little as 550 ml of pleural uid, with 100% sensitivity for effusions of 100 ml or more [10,11]. Ultrasonography has the advantage of being portable, low cost, lack of radiation exposure, and ability to perform

thickening with organization in the pleural space in only 6 patients. Therefore, real time gray scale ultrasound has a low specicity in discrimination of minimal pleural effusion from pleural thickening (33.3%) with accuracy, PPV and NPV being 67.5%, 63.6% and 85.7%, respectively (Table 3). Color Doppler chest ultrasound detected the uid color sign in 20 patients from the total of 22 patients with conrmed pleural effusion by aspiration, with a sensitivity of 90.9%. The uid color sign was absent in all patients with pleural thickening (no false positive results), and hence it results in a higher specicity of color Doppler ultrasound (specicity 100%) in discrimination of minimal pleural effusion from pleural thickening. The accuracy, PPV, NPV of color Doppler ultrasound in this situation were 95%, 100% and 90%, respectively (Table 3). Fig. 1A shows plain chest X-ray of right pleural based opacity following drainage of right empyema and Fig. 1B shows gray scale ultrasound which shows anechoic lesion compatible with pleural effusion, Fig. 1C shows color Doppler US of the same patient which shows absence of uid color sign which means pleural thickening. In Fig. 2A plain chest X-ray shows left pleural based opacity. In Fig. 2B gray scale ultrasound shows anechoic lesion compatible with pleural effusion while, in Fig. 2C color Doppler US of the same patient shows absence of uid color sign which means pleural thickening. In Fig. 3A plain chest X-ray shows left pleural based opacity. In Fig. 3B gray scale ultrasound shows anechoic lesion compatible with pleural effusion while in Fig. 3C color Doppler US of the same patient shows presence of uid color sign which conrms the presence of pleural effusion. Discussion Pleural diseases are common clinical conditions and imaging studies are the cornerstone in its management. Although chest X-ray is the initial diagnostic tool because of its availability, accuracy and low cost, it is less sensitive as at least 150 ml must be present for a pleural effusion to be detected on an upright

Table 3 Sensitivity, specicity, accuracy, PPV and NPPV of Gray scale and Color Doppler US in the studied patients.
Variable TP FP TN FN Sensitivity Specicity Accuracy PPV NPV Gray scale US 21 12 6 1 95.5% 33.3% 67.5% 63.6% 85.7% Color Doppler US 20 0 18 2 90.9% 100% 95% 100% 90%

TP = number of true positive results, FP = number of false positive results, FN = number of false negative results, TN = number of true negative results, PPV = Positive predictive value, NPV = Negative predictive value, US = ultrasound. Sensitivity = TP/TP + FN. Specicity = TN/TN + FP. Accuracy = TP + TN/TP + FP + TN + FN. Positive predictive value = TP/TP + FP. Negative predictive value = TN/TN + FN.

dynamic and real-time procedural guidance at the bedside [12]. In the current study, real time gray scale ultrasound has high sensitivity (95.5%) but low specicity in discrimination of minimal pleural effusion from pleural thickening (33.3%). On gray scale US, pleural uid appears as an anechoic lesion in the pleural space and characterized by changing its shape with respiratory movement. The presence of movable septae also conrms the presence of effusion which could be aspirated. However, loculated and minimal uid collections lack these criteria [1315]. Moreover, some pleural lesions other than uid may appear as focal echogenic lesions on gray scale US arising from the visceral or parietal pleura. Pleural thickening is an example of these lesions. So, it is important to differentiate these lesions from each other before thoracentesis and this differentiation may be difcult with gray scale US [16].

Table 2
Variable

Evaluation of the pleural effusion and pleural thickening using different modalities.
Pleural eusion (True positive + false positive) 40 33 20 22 (100%) (82.5%) (50%) (55%) Pleural thickening (True negative + false negative) 0 7 (17.5%) 20 (50%) 18 (45%)

Chest X-ray Gray scale US Color Doppler US Pleural uid aspiration US = ultrasound.

432

A.A. Hasan et al.

Figure 1 (A) Plain chest X-ray (Posteroanterior view) showed persistent right pleural based opacity following intercostals tube drainage of right empyema (Arrow). (B) Gray scale US showed anechoic lesion compatible with pleural effusion (Arrow). (C) Color Doppler US showed the absence uid color sign which means pleural thickening (Arrow).

Figure 2 (A) Plain chest X-ray (Posteroanterior view) showed minimal left pleural based opacity (Arrow). (B) Gray scale US of showed anechoic lesion compatible with pleural effusion (Arrow). (C) Color Doppler US showed the absence uid color sign which means pleural thickening (Arrow).

Figure 3 (A) Plain chest X-ray (Posteroanterior view) showed left pleural based opacity (Arrow). (B) Gray scale US showed anechoic lesion compatible with pleural effusion (Arrow). (C) Color Doppler US showed the presence of uid color sign which means pleural effusion (Arrow).

The color Doppler ultrasound is useful in such situations to evidence the presence of uid color sign which conrms the presence of uid in the pleural space [4,1719]. Tsai and Yang [17] found that the presence of an echo-free space between the visceral and parietal pleura that changes shape with respiration or contains movable strands or echo

densities on grayscale US, or displays a uid color sign on color Doppler US, indicates the presence of uid accumulation [16]. In our study the presence of pleural uid was conrmed by aspiration in 22 cases and this was considered as the gold standard for the presence of pleural uid. Moreover, Color

Color Doppler Chest Ultrasonography in diagnosing minimal pleural effusion Doppler US has higher sensitivity and specicity for detecting minimal pleural effusion (90.9% and 100%, respectively) and accuracy 95% which was in concordance with those of Wu et al. [18] where they studied 51 patients and found sensitivity 94.3% and 100% specicity of color Doppler ultrasound. In our study false negative results were reported in 2 cases which may occur if the color gain was set inappropriately low. There was no false positive result in our study as all cases with positive uid color sign had pleural effusion which could be aspirated. Also, this agreed with Kalokairinou-Motogna et al. [1] who reported that if the technical method is correct, there are no false-negative results, the uid color sign having specicity 100%. Wu et al. [4] reported a relatively high sensitivity (89.2%) and specicity (100%) of the uid color sign in detecting minimal uid collection that have been shown in a study comprising 76 patients. In the present study, despite the higher sensitivity of realtime, gray-scale for detecting minimal effusion is less specic as aspiration is failed in many cases fullling the criteria of pleural uid in gray scale scanning. Color Doppler US with its higher specicity can overcome this drawback of gray scale US. Conclusion Application of color Doppler examination increases the accuracy of real time chest ultrasound to discriminate pleural thickening from minimal pleural effusion and hence color Doppler examination proved to be a useful diagnostic tool when added to real-time gray-scale ultrasound for the diagnosis of minimal pleural effusion.

433

Acknowledgment The authors thank all the nursing staff in the Ultrasonography Unit in Chest Department, Assiut University Hospital, Egypt for their help during the study period. References
[1] M. Kalokairinou-Motogna, K. Maratou, I. Paianid, T. Soldatos, E. Antipa, A. Tsikkini, C.S. Balta, Application of color Doppler ultrasound in the study of small pleural effusion, Med. Ultrasono. 12 (2010) 1216. [2] O. Gehmacher, A. Kopf, M. Scheier, R. Bitschnau, T. Wertgen, G. Mathis, Can pleurisy be detected with ultrasound?, Ultraschall Med. 18 (1997) 214219.

[3] H.J. Chen, C.Y. Tu, S.J. Ling, et al, Sonographic appearances in transudative pleural effusions: not always an anechoic pattern, Ultrasound Med. Biol. 34 (2008) 362369. [4] R.G. Wu, P.C. Yang, S.H. Kuo, et al, Fluid color sign: a useful indicator for discrimination between pleural thickening and pleural effusion, J. Ultrasound Med. 14 (1995) 767769. [5] S. Beckh, P.L. Bolcskei, K.D. Lessnau, Real-time chest ultrasonography: a comprehensive review for the pulmonologist, Chest 122 (2002) 17591773. [6] K.J.W. Taylor, I. Ramos, D. Carter, et al, Correlation of Doppler US tumor signals with neovascular morphologic features, Radiology 166 (1988) 5762. [7] D.O. Cosgrove, J.C. Bamber, J.B. Davey, et al, Color Doppler signals from breast tumors, Radiology 176 (1990) 175180. [8] A. Yuan, D.B. Chang, C.J. Yu, et al, Color Doppler sonography of benign and malignant pulmonary masses, AJR Am. J. Roentgenol. 163 (1994) 545549. [9] E. Puddy, C. Hill, Interpretation of the chest radiograph, Contin. Educ. Anaesth. Crit. Care Pain 7 (2007) 7175. [10] O. Lababede, Effusion, Pleural Imaging, eMedicine Specialties Radiology > Chest, <http://emedicine.medscape.com/article/ 355524-imaging>, (updated 10.08.07). [11] N.M. Rahman, R.J. Davies, F.V. Gleeson, Investigating suspected malignant pleural effusion, BMJ 334 (2007) 206 207. [12] W.E. Brant, Ultrasound, Lippincott Williams & Wilkins, 2005. [13] W.M. Marks, R.A. Filly, P.W. Callen, Real-time evaluation of pleural lesions: new observations regarding the probability of obtaining free uid, Radiology 142 (1982) 163164. [14] B. Alptekin, D.T. Tran, A. Lisbon, A.M. Kaynar, Bedside ultrasonography in the differential diagnosis of pulmonary pathologies in the intensive care unit, J. Clin. Anesth. 142 (2006) 534536. [15] C.F. Chian, W.L. Su, C.F. Soh, H.C. Yan, W.C. Perng, C.P. Wu, Echogenic swirling pattern as predictor of malignant pleural effusions in patients with malignancies, Chest 126 (2004) 129134. [16] T.H. Tsai, P.C. Yang, Ultrasound in the diagnosis and management of pleural disease, Curr. Opin. Pulm. Med. 9 (2003) 282290. [17] P.C. Yang, K.T. Luh, D.B. Chang, H.D. Wu, H.D. Wu, C.J. Yu, S.H. Kuo, Value of sonography in determining the nature of pleural effusion: analysis of 320 cases, AJR Am. J. Roentgenol. 159 (1992) 2933. [18] R.G. Wu, A. Yuan, Y.S. Liaw, et al, Image comparison of real time gray-scale ultrasound and color Doppler ultrasound for use in diagnosis of minimal pleural effusion, Am. J. Respir. Crit. Care Med. 150 (1994) 510514. [19] A. Roch, M. Bojan, P. Michelet, et al, Usefulness of ultrasonography in predicting pleural effusions >500 mL in patients receiving mechanical ventilation, Chest 127 (2005) 224 232.