29

Value of Sonography in
Determining the Nature of Pleural
Effusion: Analysis of 320 Cases

Pan-Chyr Yang1 To assess the value of sonography in determining the nature of pleural eftusions, we
Kwen-Tay Luh2 prospectively analyzed the sonographic findings in 320 patients with pleural effusion of
Dun-Bing Chang1 various causes (224 with exudates and 96 with transudates). The nature of the effusions
was established on the basis of chemical, bacteriologic, and cytologic examination of
Huey-Dong Wu2
pleural fluid; pleural biopsy; and clinical follow-up. All patients had high-frequency, real-
American Journal of Roentgenology 1992.159:29-33.

Chong-Jen Yu1
time sonography performed by one of three sonographers who had no clinical informa-
Sow-Hsong Kuo2 tion concerning the patients. The sonographer evaluated the images for internal echo-
genicity of the effusion, thickness of the pleura, and associated parenchymal lesions of
the lung. The images were also printed out and interpreted a second time by the other
two sonographers to reach a consensus. Our results showed that the two types of
effusions could be distinguished on the basis of sonographic findings. Transudates
were anechoic, whereas an anechoic effusion could be either a transudate or an exudate.
Pleural effusions with complex septated, complex nonseptated, or homogeneously
echogenic patterns were always exudates (p < .01). Sonographic findings of thickened
pleura and associated parenchymal lesions in the lung also were indicative of an exudate
(p < .01). Homogeneous echogenic effusions were due to hemorrhagic effusion or
empyema. Sonographic evidence of a pleural nodule was a specific finding in patients
with a malignant effusion.
We conclude that sonography is useful in determining the nature of pleural effusion.

AJR 159:29-33, July 1992

Pleural effusions are classically divided into transudates and exudates [1 A ].

transudate is caused by systemic factors that influence the formation and absorp-
tion of pleural fluid. The pleural surfaces are not involved by the primary disease.
An exudate is caused by diseased pleural surfaces. Differentiation between a
transudate and an exudate may affect the diagnostic approach and the patients
management.
Although chest sonography has been useful for the diagnosis of pleural opacities
[2-1 0], the main use of sonography is still limited to guiding aspiration of minimal
effusions and loculated effusions. The success rate of sonographically guided
thoracentesis is high, and the procedure is safe [1 1 1 2]. Several recent studies ,

extended the use of sonography to the examination of chest wall tumors [13],
evaluation of pleural involvement by lung cancer [1 4], and guidance of a pleural
biopsy for focal pleural involvement [1 5]. The usefulness of high-frequency, real-
Received November 25, 1991; accepted after
time sonography in determining the nature of pleural effusion has not been
revision January 27, 1992.
1 Department of Intemal Medicine, National Tai-
specifically assessed before.
wan University Hospital, No. 1, Chang-Te St., Accordingly, we investigated the usefulness of sonographic findings, including
Taipei, Taiwan 100, Republic of China. Address the internal echogenicity and associated changes in the pleural and lung paren-
reprint requests to P-C. Yang. chyma, in determining the nature of pleural effusion.
2Depetment of Clinical Pathology, National Tai-
wan University Hospital, Taipei, Taiwan 100, Re-
Subjects and Methods
public of China.

0361-803x/92/1591-0029 We prospectively analyzed the value of the sonographic pattern in predicting the nature of
American Roentgen Ray Society pleural effusion in 320 consecutive patients between June 1985 and December 1989 at
 30 YANG ET AL. AJR:159, July 1992

National Taiwan University Hospital. Patients who had prior needle Tokyo) with 3.5-, 5.0-, and 7.5-MHz linear and convex transducers.
aspiration were excluded. The study included 1 89 male subjects and The sonography was performed by one of three sonographers who
1 31 female subjects, 2 and 84 years old (mean age, 54
between had no clinical information concerning the patients. The patients were
16 years). Ninety-six patients (30%) had massive effusion that in- examined while supine or sitting, with the transducer scanning
volved more than two thirds of the hemithorax on chest radiographs, through the intercostal space. The sonograms were first interpreted
1 66 patients (52%) had moderate effusion, and 58 patients (18%) by the examiner for internal echogenicity of the effusion, pleural
had minimal effusion. thickness, pleural nodules, and associated parenchymal lesions of
The nature of the effusions in the 320 patients was established on the lung. The sonograms also were recorded on Polaroid film (Pola-
the basis of chemical, bacteriologic, and cytologic examination of the roid, Cambridge, MA) and interpreted by the other two sonographers.
pleural fluid and by pleural biopsy, as well as by various hematologic If the interpretations differed, the final sonographic diagnosis was the
examinations and clinical follow-up. Each effusion was defined as a majority interpretation. The echogenicity of bile in the gallbladder was
transudate, an exudate, or an empyema on the basis of the levels of used as a reference for anechoic lesions. Echogenicity of the effusion
sugar, lactate dehydrogenase (LDH), and total protein in the effusion was compared with echogenicity of the liver (hypoechoic, isoechoic,
and the results of cytologic examinations and bacterial cultures [16]. or hyperechoic).
The pleural exudates met at least one of the following criteria, The effusion was subclassifled as anechoic, complex nonseptated,
whereas pleural transudates met none: (1) pleural fluid protein level complex septated, or homogeneously echogenic. The effusion was
divided by serum protein level greater than 0.5, (2) pleural fluid LDH defined as anechoic if echo-free spaces were present between vis-
level divided by serum LDH level greater than 0.6, and (3) pleural fluid ceral and parietal pleura, complex nonseptated if heterogeneous
LDH level greater than two thirds the upper limit of the normal level echogenic material was inside the anechoic pleural effusions, complex
of the serum LDH. Parapneumonic effusions are pleural effusions septated if fibrin strands or septa were floating inside the anechoic
associated with bacterial pneumonia orlung abscess [1 7]. Empyemas pleural effusions, and homogeneously echogenic if homogeneously
are diagnosed when accumulations of pus are seen in the pleural echogenic spaces were present between visceral and parietal pleura
space or when bacterial cultures of pleural fluid are positive. Hemor- (Fig. 1).
rhagic effusions
American Journal of Roentgenology 1992.159:29-33.

are diagnosed when fluids obtained from thoracen- The parietal pleura was measured and arbitrarily defined as thick-
tesis appear bloody and incoagulable [17]. ened if the pleural thickness was 3 mm or greater (Fig. 2). The pleural
An effusion was defined as malignant if cytologic examination of nodules were hypoechoic nodular lesions with defined margins 10-
the fluid showed malignant cells or histologic examination of sped- cated in the panetal or visceral pleura (Fig. 3), while focal pleural
mens obtained from pleural biopsy or transthoracic needle aspiration thickenings were echogenic areas of increased thickness in the
biopsy showed evidence of a malignant neoplasm. parietal pleura that had poorly defined margins. The lesions in the
The underlying diseases were diagnosed on the basis of the results lung parenchyma were subclassified into pulmonary consolidation,
of chemical, bacteriologic, and cytologic examinations of the pleural abscess, and tumor. Consolidation was seen as a wedge-shaped
effusions, chest radiographs, CT scans, biopsy from primary or hypoechoic lesion with an air bronchogram in the lung parenchyma
metastatic sites, and clinical follow-up. (Fig. 4). Lung abscess appeared as a hypoechoic cavity in a consoli-
Table 1 shows the nature of fluid in 320 patients with pleural dated lung. Tumor was a homogeneously hypoechoic or echogenic
effusions. Ninety-six effusions were transudates, and 224 were exu- mass in the consolidated lung parenchyma(Fig. 5). Associated lesions
dates. Among the 224 exudates, 1 1 3 were malignant and 1 1 1 were in the lung parenchyma shown on sonograms were confirmed either
not. Twenty-eight patients had parapneumonic effusions, 20 had on chest radiographs or CT scans of chest.
empyemas, and 1 6 had hemorrhagic effusions. Data were analyzed statistically with the chi-square test; a p value
All patients were examined with high-resolution sonographic units less than .05 was considered significant.
(Aloka SSD 630, SSD 650, Aloka, Tokyo; Toshiba 1OOA, Toshiba,

Results

TABLE 1: The Nature of Pleural Effusions in 320 Patients The sonographic patterns and the nature of the pleural
effusions in 320 patients are shown in Table 2. Four basic
Nature of Effusion No. of Patients
sonographic patterns of internal echogenicity of pleural effu-
Transudate (n = 96) sions were seen. One hundred seventy-two effusions were
Congestive heart failure 36
anechoic, 50 were complex nonseptated, 76 were complex
Ciimosis of liver 24
Nephrotic syndrome 20 septated, and 22 were homogeneously echogenic. All pleural
Hypoalbuminemia 16 effusions with an internal sonographic pattern that was com-
Nonmalignant exudate (n = 111) plex septated, complex nonseptated, and homogeneously
Parapneumonic effusion 28 echogenic were exudates (p < .01). The anechoic effusions
Tuberculous pleurisy 24
Collagen diseases 20 could be either transudates or exudates. None of the internal
Empyema 20 sonographic patterns were specific for malignant effusion. Of
Hemothorax 16 22 patients with homogeneously echogenic effusions, 10
Postpericardiotomy syndrome 3 patients had empyema and 1 2 had hemorrhagic effusions.
Malignant exudate (n = 113)
Eight of the hemorrhagic effusions were malignant.
Lung cancer 58
Breast cancer 24 Seventy-six patients had pleural thickness of 3 mm or more.
Lymphoma and leukemia 4 Only three of the effusions were transudates, the other 73
Esophageal cancer 4 effusions were exudates (p < .01). Ten patients had pleural
Gastric cancer 3 nodules on either the parietal pleura or visceral pleura de-
Colonic cancer 4
Carcinoma of unknown primary 16
tected with sonography. All of these patients had malignant
effusions. Nine of the patients had effusions with cytologic
 AJR:159, July 1992 SONOGRAPHY OF PLEURAL EFFUSION 31

Fig. 1.-A-D, Sonograms show four typical

patterns of pleural effusion: homogeneously
anechoic (A), complex nonseptated with heter-
ogeneously hyperechoic spots (arrowhead) in-
side effusion (B), complex septated with septa
or fibrin strands (arrowhead in C), and homoge-
neously echogenic (0). E = effusion, D = dia-
phragm.
American Journal of Roentgenology 1992.159:29-33.

Fig. 2.-40-year-old man with adenoid cystic

carcinoma in mouth and right-sided pleural ef-
fusion. Sonogram of chest shows massive effu-
sion (E) with complex nonseptated pattern. Pa-
rietal pleura is 4-5 mm thick (arrowheads).
Effusion study shows exudate, and cytologic
examination confirmed malignant effusion.

Fig. 3.-42-year-old man with nasopharyn-

geal carcinoma and right-sided, massive pleural
effusion. Results of repeated cytologic exami-
nations were negative for malignant cells. Son-
ogram of chest shows a 1.5-cm hypoechoic
nodule at parietal pleura (arrowhead). Sono-
graphically guided needle aspiration biopsy of
nodule revealed squamous cell carcinoma. E =
effusion, L = collapsed lung.

results positive for malignant cells. The other patient had dations, four with lung abscesses, four with obstructive pneu-
malignant effusion confirmed by needle aspiration of the monia, and six with tumor. In 32 patients with sonographic
pleuralnodule. diagnosis of pulmonary consolidation, findings on chest radio-
Fifty-four patients had pleural effusion with associated lung graphs confirmed the diagnoses. In the other 14 patients with
parenchymal changes; this included 40 patients with consoli- lung abscesses, obstructive pneumonias, and consolidations,
 32 YANG ET AL. AJR:159, July 1992

Fig. 4.-30-year-old woman with right-sided

pleural effusion. Sonogram of chest reveals a
wedge-shaped consolidation (arrowheads) with
pleural effusion (E), suggesting an exudate. This
patient was finally proved to have pneumonia
with parapneumonic effusion.

Fig. 5.-68-year-old woman with left-sided,

massive pleural effusion. Cytologic examination
of pleural effusion showed lymphocytosis and
no malignant cells. Sonogram of chest reveals a
hypoechoic tumor (arrowheads) in consolidated
lung (L) in addition to effusion (E). Sonographi-
cally guided transthoracic needle aspiration of
tumor confirmed diagnosis of squamous cell car-
cinoma.
American Journal of Roentgenology 1992.159:29-33.

TABLE 2: Sonographic Patterns and Nature of Pleural Effusion in 320 Patients

Internal Echogenicity
Thickened Pleural Parenchymal
Effusions Complex Complex Homogeneously Pleura Nodule Lesions
Anechoic
Nonseptated Septated Echogenic (n = 76) (n = 10) (n 54)
(n = 172) =
(n = 50) (n = 76) (n = 22)

Transudate
96 0 0 0 3 0 3
(n = 96)
Exudate
(n = 224)
Nonmalignant
30 27 40 14 42 0 38
(n = 111)
Malignant
46 23 36 8 31 10 13
(n = 113)

the parenchymal lesions were confirmed by both chest ra- 1 0, 21 -23]. Use of high-frequency (3.5-, 5.0-, and 7.5-MHz),
diography and CT of the chest. Fifty-one patients had exu- real-time, linear and sector transducers greatly improved the
dates and three patients had transudates (p < .05). Two of image resolution in the detection of pleural effusion. Not only
the three patients with transudates had obstructive pneu- can the internal echogenicity of a pleural effusion be visualized
monia, and one had a fibrotic infiltrate due to an inactive in more detail but the associated pleural and parenchymal
pulmonary tuberculosis. changes can be clearly depicted [1 3, 1 5]. The internal echo-
genicity of pleural effusions can be anechoic, complex non-
septated, and complex septated [5]. Also, the echogenicity
Discussion of pleural effusion can be homogeneous [1 1]. The sono-
graphic observation of pleural thickness, pleural tumor, and
The value of sonography for the detection of pleural lesions associated lung parenchymal changes have not been consid-
is well known [2-1 2]. Sonography is useful in defining the ered together with the internal echogenicity of pleural fluid as
nature of pleural masses [5, 8, 9, 1 8] and localizing loculated criteria for determining the nature of pleural effusions [5, 1 1,
or minimal effusion before thoracentesis [5, 7, 1 1 , 12]. Re- 24].
cently, chest sonography has been found useful in detecting Our results show that sonography can be used to determine
pleural and pleurally based lesions [7], evaluating pleural the nature of pleural effusion. In addition to the basic effusion
involvement by lung tumor [1 3], assessing lesions in lung patterns (anechoic, complex nonseptated, and complex sep-
parenchyma, and guiding percutaneous transthoracic biopsy tated [5]), a pleural effusion can be homogeneously echo-
[15, 19, 20]. genic. Transudates are usually anechoic, whereas an ane-
Previous studies on the use of sonography to determine choic effusion could be either a transudate or an exudate.
the nature of pleural effusions are limited [2-9]. Most of the Pleural effusions with complex septated, complex nonsep-
reported studies were done with contact B-scans [2, 3, 6- tated, or homogeneously echogenic patterns are always ex-
 AJR:159, July 1992 SONOGRAPHY OF PLEURAL EFFUSION 33

udates (p < .01). An echogenic effusion may sometimes be 3. Laing FC, Filly RA. Problems in the application of ultrasonography for the
evaluation of pleural opacities. Radiology 1978;126:21 1-214
confused with a solid lesion. However, if the lesion changes
4. Rosenberg ER. Ultrasound in the assessment of pleural densities. Chest
shape with respiration and tiny echogenic materials can be 1983;84:283-285
seen swirling, then the lesion is fluid [1 1]. In this series, the 5. Hirsch JH, Rogers JV, Mack LA. Real-time sonography of pleural opacities.
homogeneously echogenic effusions are seen in hemorrhagic AJR 1981;136:297-301
6. Marks WM, Filly RA, Callen PW. Real-time evaluation of pleural lesions:
effusions and empyema only. The echogenic nature is prob-
newobservations regarding the probability ofobtaining freefluid. Radiology
ably due to the presence of a high content of tissue debris or 1982;142: 163-164
blood in the pleural cavity [1 1]. Patients with homogeneously 7. Yang PC, Sheu JC, Luh KT, Kuo SH, Yang SP. Clinical appliCatiOn of real-
echogenic effusions may need drainage via a chest tube. The time ultrasonography in pleural and subpleur& lesions. J Formosan Med
associated thickened pleura and lung parenchymal changes Assoc 1984;83:646-657
8. Lipscomb DJ, Flower CDR. tJtrasound in the diagnosis and management
are also indicative of exudates. The presence of a pulmonary
of pleural disease. Br J Dis Chest 1980;74:353-361
consolidation or lung abscess may suggest an exudate of 9. Hirsch JH, Carter SJ, Chikos PM, Calacurcio C. (Jtrasonic evaluation of
infectious origin. Presence of tumor in the consolidated lung radiographic opacities of the chest. AiR 1978;130: 1153-1156
may indicate a malignant lesion involved in the pathogenesis 10. Ravin CE. Thoracocentesis of loculated pleural effusions using grey scale
of effusion. The pleural nodules were seen only in patients ultrasonic guidance. Chest 1977;71 :666-668
1 1 . McLoud TC, Flower CDR. Imaging the pleura: sonography, CT, and MR
with malignant effusions in this series.
imaging. AiR 1991;156: 1145-1153
Fibrin strands and septa within a hypoechoic space are 12. Henschke CL. The pathogenesis, radiologic evaluation and therapy of
useful signs serving to distinguish pleural fluid from a solid pleural effusion. Radiol Clin North Am 1989;27: 1241 -1 255
mass [6, 1 1 , 24]. The fibrin strands tend to occur in effusions 13. Saito T, Kobayashi H, Kitamura S. Ultrasonographic approach to diagnos-
ing chest wall tumors. Chest 1988;94: 1271 -1 273
that are rich in protein [1 1]. The winding bands or fibrin
14. Sugama Y, Tamaki 5, Kitamura S, Kira S. %Jtrasonographic evaluation of
strands also were reported to associate with tuberculous pleural and chest wall invasion. Chest 1988;93:275-279
American Journal of Roentgenology 1992.159:29-33.

pleural effusions [24]. In this study, we found that fibrin 15. Chang DB, Yang PC, Luh KT, Kuo SH, Yu CJ. (Jtrasound-guided pleural
strands and septa were commonly seen in all kinds of exu- blopsy with tru-cut needle. Chest 1991;100:328-333
16. Light RW, MacGregor MI, Luchsinger PC, Ball WC. Pleural effusions: the
dates, including empyema, hemothorax, parapneumonic ef-
diagnostic separation of transudate and exudates. Ann Intern Med 1972;
fusions, and malignant pleural effusions. Sometimes the septa
77:507-513
were so profuse that they had a honeycomb appearance. 17. Light RW. Pleural diseases, 2nd ed. Philadelphia: Lea & Febiger, 1990:
In addition to the useful diagnostic information provided by 39-73
the sonograms, chest sonography also can be used to guide 18. Wu HD, Yang PC, Kuo SH, Luh KT. tJtrasonography in complete chest x-
ray opacification of hemithorax. J Formosan MedAssoc 1989;88:694-699
a percutaneous transthoracic needle aspiration biopsy of the
19. Yang PC, Luh KT, Wu HD, et al. Lung tumors associated with obstructive
associated pleural and lung parenchymal lesions with high pneumonitis: US studies. Radiology 1990;174:717-720
diagnostic yield [15, 19, 20]. 20. Yang PC, Luh KT, Lee YC, et al. LJtrasonography and ultrasound-guided
We conclude that sonography is a useful diagnostic tool transthoracic aspiration of lung abscess. Radiology 1991;180: 171 -1 75
for determining the nature of pleural effusions. 21 . Gryminski J, Krakowka P, Lypacewicz G. The diagnosis of pleural effusion
by ultrasonic and radiographic techniques. Chest 1976;70:33-37
22. Sandweiss DA, Hanson JC, Gosink BB, Moser KM. tjtrasound in diagno-
REFERENCES sis, localization, and treatment of loculated pleural empyema. Ann Intern
Med 1975;82:50-53
1. Paddock FK. The diagnostic significance of serous fluids in disease. N 23. Joyner CR Jr, Herman RJ, Reid JM. Reflection ultrasound in the detection
EnglJ Med 1940;223:1010-1015 and localization of pleural effusion. JAMA 1967;200:399-402
2. Doust BD, Baum JK, Maklad NF, Doust VL. tJtrasonic evaluation of pleural 24. Martinez DC, Serrano By, Romero RR. Real-time ultrasound evaluation of
opacities. Radiology 1975;1 14:134-140 tuberculous pleural effusions. JCU 1989;17:407-410