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(Chest. 2004;126:1274-1280.)
© 2004 American College of Chest Physicians

Pleural Effusions in Febrile Medical ICU Patients*

Chest Ultrasound Study

Chih-Yen Tu, MD; Wu-Huei Hsu, MD, FCCP; Te-Chun Hsia, MD; Hung-Jen Chen, MD; Kuen-Daw Tsai, MD; Chung-Wen Hung, MD and Chuen-Ming Shih, MD

* From the Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan.

Correspondence to: Wu-Huei Hsu, MD, FCCP, Department of Internal Medicine, China Medical University Hospital, Taichung, Taiwan; e-mail: hsuwh{at}www.cmuh.org.tw


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To assess the necessity of thoracentesis in febrile medical ICU (MICU) patients, and to evaluate the efficiency and reliability of sonographic effusion patterns for diagnosing empyema.

Design and setting: A prospective, 1-year, tertiary-care hospital study of febrile MICU patients with physical, radiographic, and ultrasonographic evidence of pleural effusion.

Patients: During this study period, we screened 1,640 patients who had been admitted to the MICU; of these, 94 patients had a temperature > 38°C for > 8 h with evidence of pleural effusion proven by chest radiography and ultrasound.

Intervention: Routine thoracentesis and pleural effusion cultures were performed in 94 febrile patients under portable chest ultrasound guidance. Three days later, if the first pleural effusion culture was inconclusive and the patient still had persistent fever of > 38°C, we repeated the diagnostic thoracentesis and pleural effusion culture. In total, 118 procedures were performed in those 94 febrile patients.

Measurements and results: In all, 58 patients (62%) had infectious exudates (parapneumonic, n = 36; empyema, n = 15; urosepsis, n = 3; liver abscess, n = 2; deep neck infection, n = 1; and wound infection, n = 1), 28 patients (30%) had transudates, and 8 patients (8%) had noninfectious exudates. The prevalence of empyema in febrile patients admitted to the MICU was 16% (15 of 94 patients). Analyses of the sonographic patterns of the 15 patients with empyema out of the 118 thoracenteses performed showed the following: anechoic pattern, 0% (0 of 47 procedures); complex nonseptated and relatively nonhyperechoic pattern, 0% (0 of 36 procedures); complex nonseptated and relatively hyperechoic pattern, 100% (2 of 2 procedures); complex septated pattern, 35% (11 of 31 procedures); and homogenously echogenic pattern, 100% (2 of 2 procedures). Hemothorax was the only complication, and it occurred in two patients (2%). Both patients had a favorable outcome after drainage.

Conclusion: Portable chest ultrasound examination and ultrasound-guided thoracentesis in febrile MICU patients are safe, feasible, and useful methods for diagnosing thoracic empyema. Our results suggest that only some sonographic patterns of pleural effusion (homogenously echogenic, complex nonseptated and relatively hyperechoic, and complex septated) deserve aggressive assessment and rapid management.

Key Words: empyema • ICU • pleural effusion • thoracentesis • ultrasound


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Pleural effusions in medical ICU (MICU) patients are usually caused by pulmonary or extrapulmonary disorders, rather than by primary pleural diseases. Most pleural effusions in MICU patients are sterile. However, once a MICU patient’s condition progresses to an empyema, early diagnosis and therapy are important to improve the prognosis.1 However, few studies123 have proposed precise guidelines about early diagnosis and detection of empyema in febrile MICU patients.

The prevalence and clinical significance of empyema in febrile MICU patients are unknown. Pleural effusions are often present in ICU patients, and they are frequently uncomplicated, but empyema is relatively uncommon; when it is encountered, it appears to be resistant to antibiotic treatment alone in the ICU. In fact, the prevalence of empyema is probably underestimated. MICU patients are often immobile because of pain, sedation, or paralytic drugs, which puts them at risk of delayed detection of empyema. The incidence of empyema in MICU patients with pleural effusions ranges from 2 to 17.3%.12 Because most pleural effusions are sterile rather than empyemic, the necessity of routine thoracentesis and examination of pleural fluid in febrile MICU patients must be reexamined.

Chest ultrasound is a safe, convenient, and effective method even for assessing diagnostic puncture of small pleural effusions in patients receiving mechanical ventilation.45 The sonographic patterns of pleural effusions are also useful for differentiating a transudate from an exudate: a transudate usually has an anechoic sonographic appearance, whereas exudates can have an anechoic, complex (either complex septated, or complex nonseptated), or echogenic appearance.67

In this article, we report our results of a prospective, 1-year study of chest ultrasound examinations in febrile MICU patients who had pleural effusions and underwent thoracentesis. The aims of the study were to evaluate the necessity of thoracentesis in febrile MICU patients with pleural effusion, and to assess the prevalence of empyema and study the sonographic patterns of these patients.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
From April 1, 2001, to March 31, 2002, all consecutive patients admitted to the MICU (44 beds in all in our hospital) with fever > 38°C for > 8 h were screened prospectively for physical and radiographic evidence of pleural effusion. In general, pleural effusion was suspected in these febrile ICU patients based on routine chest radiographs obtained in the supine position. During the 1-year study period, 1,640 patients were admitted to our MICU; of these, 94 febrile patients with pleural effusions proven by chest radiography and ultrasound and undergoing thoracentesis under ultrasound guidance were enrolled in our series. The 94 patients consisted of 55 men and 39 women (age range, 22 to 92 years; mean age, 66 ± 19 years [ ± SD]). Seventy-six patients had underlying chronic diseases and/or received long-term drug treatment; the remaining 18 patients were healthy before admission.

Study Design and Data Acquisition
A bedside portable chest ultrasound device (Toshiba SSA-220A; Toshiba Corporation; Tokyo, Japan) was routinely performed on each MICU patient who had fever > 38°C for > 8 h and was suspected of having pleural effusion based on physical and radiographic evaluation. Chest ultrasound examination and ultrasound-guided thoracentesis were performed after obtaining informed consent from, and explaining the clinical condition to, the patients themselves and/or their families. When a pleural effusion was confirmed by ultrasound examination, we elevated and adjusted the patient from a supine position to a 45°, semirecumbent position. A fine needle (18 to 22 gauge) was inserted at the appropriate intercostal space for the aspiration of the effusion from either the dorsal or lateral chest wall. Before performing the ultrasound-guided fluid aspiration, the sonographic pattern of each pleural effusion was recorded and printed on sonopaper. The pleural fluid samples were collected and sent for the following investigations: total and differential cell counts, biochemistry, Gram stain and bacterial culture, acid-fast bacilli smear examination, and mycobacterial culture. Three days later, if the results of the first aspirated pleural effusion were still inconclusive, and the patient still had persistent fever > 38°C without clinical improvement, repeated thoracentesis and pleural fluid studies were performed. Ultrasound rescreening of the chest was done for pneumothorax and hydropneumothorax after each thoracentesis, and radiographic examination was performed the following day.

Classification of Sonographic Patterns in Pleural Effusions
We collected the sonograms of all 94 enrolled patients and classified them into five groups based on the appearance of pleural effusion, as follows (Fig 1 ): I: anechoic pattern: no echogenic density within the effusion; IIA: complex nonseptated and relatively nonhyperechoic pattern, with some visible bright spots as echogenic density within the effusion and the echogenic shape changed with respiration; IIB: complex nonseptated and relatively hyperechoic pattern, with hyperechoic spots prominently deposited within the effusion, and the echogenic shape not changed with respiration; III: complex septated pattern, with prominent fibrinous septation within the effusion; and IV: homogenously echogenic pattern, with echogenic spot density evenly distributed within the effusion.



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  		Figure 1.. Five basic ultrasound patterns of pleural effusions. Top left, I = anechoic pattern: no echogenic density within the effusion; Top right, IIB = complex nonseptated and relatively nonhyperechoic pattern: some visible bright spots as echogenic density within the effusion, and the echogenic shape changed with respiration; Center left, IIA = complex nonseptated and relatively hyperechoic pattern: predominant hyperechoic spots visible within the effusion, and the echogenic shape not changed with respiration; Center right, III = complex septated pattern: prominent fibrinous septation visible within the effusion; Bottom, IV = homogenously echogenic pattern: echogenic spots density evenly distributed within the effusion. Arrowheads indicate a homogenously echogenic pleural effusion (D = diaphragm).

 
Definitions of Pleural Effusions and Underlying Diseases
The cause of pleural effusion was determined based on clinical findings (presumptive diagnosis) and on the results of thoracentesis (definitive diagnosis). Exudates were defined by the criteria proposed by Light et al8: pleural fluid/serum protein ratio > 0.5 and/or pleural fluid/serum lactate dehydrogenase (LDH) ratio > 0.6 and/or pleural fluid LDH greater than two thirds the upper limit of normal for serum LDH (200 IU/L).

The criteria for diagnosing the causes of pleural effusions were as follows: (1) parapneumonic effusion, a clinically documented pneumonia with loculated polymorphonuclear predominant exudate pleural fluid910; (2) empyema, with aspirated effusion showed flank pus, a positive pleural fluid culture finding, or Gram stain for microorganism11; (3) heart failure, with S3 gallop rhythm and basal crackles, with chest radiography showing cardiomegaly, pulmonary congestion, and usually bilateral effusions; (4) urinary tract infection (UTI), a compatible clinical presentation of UTI with symptoms and signs of sepsis, chest radiography showing no parenchymal infiltrate, and resolution of the effusion after the sepsis resolved; (5) hypoalbuminemia, a transudative effusion in patients with a serum albumin level < 25 g/L; (6) liver abscess, with clinical, laboratory, and imaging evidence of liver abscess and the effusion resolved as the liver abscess resolved; (7) pancreatic effusions, with clinical, radiographic, and biochemical evidence of documented pancreatitis and the effusion resolves as the pancreatitis resolved; (8) hepatic hydrothorax, a transudative effusion in patients with a history of liver cirrhosis and ultrasound-documented ascites; (9) lupus pleural effusion, an exudative pleural effusion, in patients with a confirmed diagnosis of systemic lupus erythematosus (SLE), where no other cause is apparent; (10) deep neck infection, with clinical and radiographic picture compatible with deep neck infection and the effusion resolved after the infection was controlled; (11) wound infection, in which patients have a wound infection and bacteremia but the chest radiograph shows no pulmonary infiltrations; and (12) malignant pleural effusion, an exudative effusion with positive malignant cells found by cytologic examination.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Demographic Data
Of the 1,640 patients admitted to our MICU during the 1-year study period, 94 febrile patients with pleural effusions underwent a total of 118 thoracenteses under chest ultrasound guidance, yielding an annual incidence of 5.7% thoracentesis in febrile MICU patients. Respiratory failure was the most common cause for MICU admission, and 81 patients (86%) were receiving mechanical ventilation at the time of thoracentesis. The demographic features of the 94 enrolled patients with diverse primary diseases are summarized in Table 1 . Of those enrolled in this study, no patients were admitted to the MICU due to primary pleural diseases.


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  		Table 1.. Clinical Characteristics of the 94 Enrolled Febrile Patients With Pleural Effusions Admitted to the MICU*

 
Sonographic Patterns of Pleural Effusions
The effusions contained infectious exudates (exudative pleural effusions caused by underlying infectious diseases, including parapneumonic, empyema, urosepsis, liver abscess, deep neck infection, and wound infection) in 58 patients (62%), noninfectious exudates (exudative pleural effusions not caused by infectious diseases) in 8 patients (8%), and transudates in 28 patients (30%). Pleural effusion was caused by uncomplicated parapneumonic effusion in 38% (36 of 94 patients), empyema in 16% (15 of 94 patients), heart failure in 10% (9 of 94 patients), sepsis from UTI in 9% (8 of 94 patients), hypoalbuminemia in 7% (7 of 94 patients), liver abscess in 3% (3 of 94 patients), pancreatitis in 2% (2 of 94 patients), hepatic hydrothorax in 2% (2 of 94 patients), SLE in 1% (1 of 94 patients), sepsis from deep neck infection in 1% (1 of 94 patients), sepsis from wound infection in 1% (1 of 94 patients), malignant pleural effusion in 1% (1 of 94 patients), and unknown origin in 9% of those enrolled (8 of 94 patients). Most infectious exudates (88%; 51 of 58 exudates) were attributed to pulmonary parenchymal infection. Table 2 shows the results in detail.


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  		Table 2.. Causes and Characteristics of Pleural Effusions in 94 Patients Admitted to the MICU

 
Fifteen procedures diagnosed empyema in the 118 thoracentesis performed, yielding an incidence of 12.7% (15 of 118 procedures) for a positive pleural effusion culture finding. Of these 15 patients with proven empyema, 12 cases were diagnosed at the first thoracentesis. The remaining three cases were diagnosed at the second thoracentesis. The diagnostic protocol and the results of proven empyema are listed in Figure 2 .



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  		Figure 2.. Results of the diagnostic protocol and the sonographic effusion patterns in empyema. Sonographic patterns are as follows: I, anechoic pattern; IIA, complex nonseptated and relatively nonhyperechoic pattern; IIB, complex nonseptated and relatively hyperechoic pattern; III, complex septated pattern; and IV, homogenously echogenic pattern. N* = no growth.

 
As shown in Figure 2 and Table 3 , we also collected and analyzed the sonographic patterns of the 118 pleural effusions. Interestingly, 40% of the sonographic patterns of the pleural effusions were anechoic pattern (47 of 118 effusions), and 31% were complex nonseptated and relatively nonhyperechoic pattern (36 of 118 effusions), which did not affect the patients’ management. All of the 15 patients with thoracic empyema had distinct sonographic patterns, including complex nonseptated and relatively hyperechoic pattern in 2 patients (2 of 2 procedures; 100%), complex septated pattern in 11 patients (11 of 31 procedures; 35%), and homogenously echogenic pattern in 2 patients (2 of 2 procedures; 100%). Therefore, most febrile patients with pleural effusions who present with common sonographic patterns (anechoic, complex nonseptated, and relatively nonhyperechoic patterns) might not require immediate thoracentesis.


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  		Table 3.. Analysis of Sonographic Patterns in 118 Pleural Effusions and 15 Thoracic Empyema Cases*

 
Bacteriology of Empyema
In our series, the incidence of empyema in febrile MICU patients was 16% (n = 15; 15 of 94 patients; 16%). The presumptive causes of empyema were parapneumonic effusion (n = 14) and septic emboli (n = 1). The microbiological diagnoses of causative microorganisms of thoracic empyema are summarized in Table 4 .


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  		Table 4.. Demographics, Clinical Data, Bacteriology, and Sonographic Patterns of Pleural Effusions in 15 Patients With Empyema*

 
Complications
Hemothorax occurred in two patients after ultrasound-guided thoracentesis, with the complication rate at approximately 2%. The hemothorax improved after adequate drainage. No occurrence of pneumothorax appeared in our series.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Empyema is a potentially life-threatening complication in the MICU. A good outcome demands prompt recognition, appropriate antibiotic therapy, and adequate pleural drainage. However, thoracic empyema might be missed or detected late in the ICU, particularly for patients receiving mechanical ventilation. Previous studies12 have focused on routine thoracentesis to diagnose pleural effusion in MICU patients. To our knowledge, no study has evaluated using sonographic effusion patterns to help diagnose empyema in febrile MICU patients. From our present study and experience, chest ultrasound examination and ultrasound-guided thoracentesis are safe and useful for critical patients undergoing thoracentesis, and sonographic patterns of pleural effusions can further help in early detection of empyema development.

As reported in the literature and in our series, the majority of pleural effusions that occur in the febrile patients are parapneumonic effusions (in our series: uncomplicated parapneumonic effusion [n = 36] and empyema [n = 15]). As known, patients who follow a complicated course with the development of empyema may progress through three phases of empyema formation.12 These three phases, which are not sharply defined but rather represent a continuous spectrum, are the exudative, fibrinopurulent, and organizing phases. Generally speaking, antibiotic therapy is most effective if initiated in the exudative phase, because there is no bacterium found and it is usually sterile in the first phase. In the second phase, fibrin is deposited as continuous sheets that cover both the visceral and the parietal pleura in the involved area. This phase is characterized by infection of the previously sterile pleural fluid with the offending bacteria, but patients in the early fibrinopurulent phase of empyema formation may also respond to antibiotics. Once a patient progresses to an organized empyema, fibroblasts grow into the exudate from both the visceral and the parietal pleural surfaces to produce an inelastic membrane, which is sometimes called a pleural peel. Surgical intervention with tube drainage is often required with a thoracotomy because of the presence of pleural peels and thick pleural membranes that trap the lung.

In our experience, chest ultrasound not only detects the fibrin as numerous fibrinous septa within the pleural effusion easily, but also can reveal the high-density cellular debris in empyema as hyperechoic spots that do not move with respiration. Therefore, the sonographic appearance of fibrin and necrotic debris within parapneumonic effusions has been associated with the development of an empyema.13

Another key finding in our series came during further analysis of sonographic patterns in 118 aspirated pleural effusions. As shows in Table 3, the pleural effusions in the exudative phase are sterile, and often present as anechoic or complex nonseptated and relatively nonhyperechoic sonographic patterns. In contrast, among pleural effusions that present as complex septated pattern, complex nonseptated and relatively hyperechoic pattern, or homogenously echogenic pattern, the incidence of diagnostic empyema is approximately 43% (empyema, n = 15; total procedures, n = 35), which is much higher than the incidence of positive effusion culture findings in all 118 thoracentesis (13%; 15 of 118 effusions). Therefore, our results suggest that sonographic patterns of pleural effusions in febrile patients admitted to MICU can be classified into two categories: (1) anechoic or complex nonseptated and relatively nonhyperechoic pattern; immediate thoracentesis with effective effusion cultures is very limited; and (2) complex septated, homogenously echogenic or complex nonseptated and relatively hyperechoic pattern; these cases require immediate thoracentesis with aggressive routine effusion examinations and cultures.

In some cases, repeated thoracenteses may be required to diagnose empyema. Our results show that the progression from uncomplicated parapneumonic effusion to an empyema is not sharply defined as three phases, but rather represent a continuous spectrum. For example, as Figure 2 shows, three patients initially presented with sterile pleural effusions, but empyema was diagnosed only after a second thoracentesis performed 3 days later. In all three patients, the sonographic effusion patterns changed between the first and the second thoracentesis; one patient with the sonographic pattern of pleural effusion changed from complex nonseptated and relatively nonhyperechoic to complex septated, and two patients changed from anechoic to complex septated. How often should one proceed with the evaluation of an effusion so as not to miss an empyema? In our limited experience, we suggest the following. If anechoic or complex nonseptated and relatively nonhyperechoic sonographic effusion patterns are encountered, a careful waiting approach is enough. If the effusion patterns change from anechoic or complex nonseptated and relatively nonhyperechoic to complex septated, homogenously echogenic, or complex nonseptated and relatively hyperechoic, aggressive intervention with a series of effusion studies is necessary to diagnose empyema. We emphasize that sequential follow-up sonography is necessary in those patients with persistent fever.

Pneumothorax should be the first concern in patients undergoing thoracentesis, especially in patients receiving mechanical ventilation.14 Nevertheless, no pneumothorax occurred in our series, even most patients (81%) receiving mechanical ventilation. Although there were still two patients with hemothorax after the ultrasound-guided thoracentesis, they both had no hemodynamic instability after the thoracentesis, and the complication was early detected by close radiographic follow-up with repeated thoracentesis. Clinically, the hemothorax improved rapidly after adequate drainage. In our series, the risk of procedure associated with ultrasound-guided thoracentesis is low and acceptable; however, for patients in ICU with relatively high risk of pneumothorax or hemothorax, close radiographic and sonographic follow-up after thoracentesis is warranted.1415

In conclusion, the development of pleural effusion in febrile patients admitted to the MICU is common, and an aggressive approach may be necessary for those in critical condition. Portable chest ultrasound provides useful imaging information and can help guide thoracentesis. In our limited experience, chest ultrasound examination and ultrasound-guided thoracentesis are safe, convenient, and useful modalities for detecting and diagnosing thoracic empyema in the early stages. Sonographic effusion patterns provide further valuable imaging information. It deserves wide clinical application in critical care medicine.


   Footnotes
 
Abbreviations: LDH = lactate dehydrogenase; MICU = medical ICU; SLE = systemic lupus erythematosus; UTI = urinary tract infection

Received for publication July 28, 2003. Accepted for publication April 21, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  14. Gervais, D, Petersein, A, Lee, M, et al Ultrasound guided thoracentesis: requirement for post-procedure chest radiography in patients who receive mechanical ventilation vs patients who breathe spontaneously. Radiology 1997;204,503-506[Abstract/Free Full Text]
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