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(Chest. 2004;125:156-159.)
© 2004 American College of Chest Physicians

Clinical Implications of Appearance of Pleural Fluid at Thoracentesis*

Victoria Villena, MD; Angel López-Encuentra, MD; Ricardo García-Luján, MD; José Echave-Sustaeta, MD and Carlos José Álvarez Martínez, MD

* From the Respiratory Service, Hospital 12 de Octubre, Madrid, Spain.

Correspondence to: Victoria Villena, MD, Servicio de Neumología, Hospital 12 de Octubre, Avda. de Córdoba s/n 28041, Madrid, Spain; e-mail: mvg01m{at}saludalia.com


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The aims of this study were to describe the different appearances of pleural fluid during thoracentesis and their frequency in relation to diagnosis, and to evaluate the causes and clinical implications of bloody pleural effusions.

Setting: Tertiary care, university-affiliated hospital.

Subjects and methods: Seven hundred fifteen patients with pleural effusion were prospectively assessed from December 1991 to December 1997.

Interventions: The appearance of the fluid was assessed in a glass assay tube containing 10 mL of pleural fluid.

Results: The most common presentations were serous and blood tinged, with 80% of the fluids fitting into one of these categories. The most frequent cause of watery fluid was transudate, although most transudates were classified as serous effusions. There were 59 bloody and 656 nonbloody pleural fluids. The most common cause of bloody pleural effusion (BPE) was malignancy (47%). Fluid with a bloody appearance slightly increased the probability of malignancy in our series (odds ratio [OR], 1.73; 95% confidence interval [CI], 1.01 to 2.94; p = 0.04). Nevertheless, only 11% of the neoplastic effusions were BPE. Other common causes of BPE were posttraumatic (12%) or parapneumonic (10%) pleural effusions. Tuberculosis and transudates were uncommon causes of BPE. Fluid that was bloody in appearance decreased the probability for both diseases (OR, 0.15; 95% CI, 0.04 to 0.57; p = 0.003 and OR, 0.25; 95% CI, 0.06 to 0.95; p = 0.04, respectively).

Conclusions: Serous and blood tinged were the most common presentations of pleural fluid at thoracentesis. Almost half of BPEs were secondary to neoplasms, but only 11% of the neoplastic effusions were BPEs. Other common causes of BPE were parapneumonic and posttraumatic.

Key Words: bloody appearance • malignant pleural effusion • pleural effusion


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
In order to determine the etiology of pleural effusions, it has been widely recommended to assess the appearance of pleural fluid at thoracentesis.1 Pleural effusions that are bloody in appearance have been particularly associated with malignant etiologies.2 Nevertheless, as far as we know, a systematic approach to pleural fluid presentation at thoracentesis within a large unselected series of patients has not been previously reported. The aims of this study were to describe the different appearances of pleural fluid during thoracentesis and their frequency in relation to diagnosis, and to evaluate the causes and clinical implications of bloody pleural effusion (BPE).


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
We prospectively studied 766 consecutive patients with pleural effusion who were assessed in our service from December 1991 to December 1997. Pleural fluid was obtained by thoracentesis with a needle. The macroscopic appearance of the fluid during thoracentesis was assessed within a glass assay tube with an internal diameter of 14 mm containing 10 mL of pleural fluid. Whenever the pleural fluid became more blood tinged during thoracentesis, the clearer color was contemplated. Fluid appearance was classified into eight categories: watery (light yellow), serous (yellow), blood tinged (reddish), bloody (dark red, similar to blood), purulent (pus), milky (white and less thick than pus), turbid (yellow, but viscous or cloudy), and others (brownish, black, etc.)

In 224 of the first 274 pleural fluids, interobserver agreement when classifying the pleural fluid into BPE and nonbloody pleural fluid was assessed. The {kappa} coefficient was 0.88. All patients were studied according to the same diagnostic algorithm.3 After completion of clinical evaluation, pleural effusions were classified into diagnostic groups based on explicit previously reported criteria4 :

Malignant:
Pleural effusions were malignant if there was either a cytologic or histologic diagnosis of neoplasm within the pleural space.

Paramalignant:
Pleural effusions were paramalignant when a histologic diagnosis of malignant tumor in another organ was established, the effusion did not meet the malignant criteria, and no other cause of pleural effusion was found.

Tuberculosis:
Pleural effusions were tuberculous if a positive Mycobacterium tuberculosis culture finding of pleural fluid or tissue and/or presence of granulomas in the pleural biopsy were found, in the absence of other pleural granulomatous diseases. This group also included 11 patients with high interferon-{gamma} levels in pleural fluid, favorable clinical course after tuberculous treatment, and either microbiological evidence of extrapleural tuberculosis or clinical picture suggestive of pleural tuberculosis.5

Parapneumonic:
Pleural effusions were parapneumonic in patients with cough, fever, and a radiographic pulmonary infiltrate that disappeared with antibiotic treatment. Empyema was defined as pus in the pleural space.

Transudate:
Pleural effusions were transudate if defined according to clinical and classic biochemical criteria.1

Other Benign Diseases:
Pleural effusions were other benign diseases if diagnosed on the basis of standard criteria.1

Undetermined or Mixed Causes:
Pleural effusions were undetermined or mixed causes whenever the etiology of the effusion was unknown or there were several potential causes of the pleural effusion.

Statistical Analysis
The Kolmogorov-Smirnov test was used to check the normal distribution of the data. The strength of the associations has been estimated as odds ratio (OR), and {chi}2 test with the Yates correction or the Fisher exact test were used as appropriate. The Mann-Whitney test or the Student t test were used to compare the differences between continuous variables; p < 0.05 was considered statistically significant. Interobserver agreement was measured by {kappa} coefficient.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The appearance of the pleural fluid was assessed in 715 of 766 patients (93.3%); 479 were male (67%) and 236 were female. Mean age was 63 years (range, 14 to 95 years). Presentations of the pleural fluid and their diagnoses are shown in Table 1 . The most common appearances were serous and blood tinged, with 80% of the fluids fitting into one of these categories. There were eight milky pleural fluids, seven of which were chylothorax and the remaining one a pseudochylothorax. The chylothorax was secondary to non-Hodgkin lymphomas (n = 3), liver cirrhosis (n = 2), tuberculosis (n = 1), or idiopathic (n = 1) and the pseudochylothorax to rheumatoid arthritis. The most frequent cause of watery fluid was transudate, although most transudates were classified as serous effusions. There was a statistically significant difference between the mean pleural fluid protein level in the transudates classified as either watery or serous (1.65 g/dL vs 2.65 g/dL, respectively; p = 0.001). There were two pleural fluids classified in the group of "others." Both were a brownish pleural fluid, due to pneumonia in one case and to chronic pancreatitis with a pancreatic pseudocyst in the other; the RBCs in the fluid were 10,000/µL and 20,000/µL, respectively.


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  		Table 1. Appearance of Pleural Fluid and Diagnoses in 715 Patients*

 
The etiologies of the BPE are reported in Table 2 . There were 59 bloody and 656 nonbloody pleural fluids. The most common cause of BPE was malignancy (47%). Fluid with a bloody appearance slightly increased the probability of malignancy in our series (OR, 1.73; 95% confidence interval [CI], 1.01 to 2.94; p = 0.04). Nevertheless, only 11% of the neoplastic effusions were BPE. Tables 3 , 4 show the origin and histologic types of the malignant effusions classified according to the bloody nature of the fluid. In the BPE group, the most common origins were the pleura and the lung, and the most common histologic types were adenocarcinoma and mesothelioma. In the malignant group, there were no statistically significant differences in the sensitivity of the first cytology (0.27 vs 0.37) or pleural biopsy (0.50 vs 0.51) between BPE and nonbloody pleural effusions.


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  		Table 2. Etiologies of the Pleural Effusions According to Fluid Color*

 

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  		Table 3. Origins of the Tumors According to Pleural Fluid Colors*

 

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  		Table 4. Histologic Type of the Tumors According to Pleural Fluid Color*

 
Other common causes of BPE were posttraumatic (12%) or parapneumonic (10%) pleural effusions. In the group of patients with postcardiac injury syndrome, one patient with internal mammary artery graft surgery had BPE, while one patient with pleural effusion after cardiac surgery and another patient after myocardial infarction had blood-tinged and serous effusion, respectively.

Tuberculosis and transudates were uncommon causes of BPE. Fluid that was bloody in appearance decreased the probability for both diseases (OR, 0.15; 95% CI, 0.04 to 0.57; p = 0.003 and OR, 0.25; 95% CI, 0.06 to 0.95; p = 0.04, respectively).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Pleural fluid appearance has been proposed as a guide for the differential diagnosis of pleural effusions.1 Nevertheless, to our knowledge, a systematic approach to the causes and clinical implications in a large, unselected series of cases has not been previously reported.

Most effusions from all the diagnostic groups were either serous or blood tinged. In the group of transudates, only 13%, with a lower concentration of proteins in pleural fluid, were classified as watery. A watery appearance was very suggestive of transudate, but most transudates were serous, and these can even look blood tinged, bloody, or turbid.

It has been suggested that the bloody presentation of an effusion increases the probability of malignancy of the pleural effusion. In our series, almost half of the patients with BPE had neoplasms. This ratio agrees with Light’s personal experience,1 but would probably be different in a surgical setting, where traumatic etiologies of the pleural effusions would be more likely. Nevertheless, a wide variety of causes can produce BPE, and fluid that is bloody in appearance, even if only slightly, increases the probability of malignancy (OR, 1.73). However, BPE, rather than being a common feature of neoplastic effusions, constituted only 11% of the neoplastic pleural effusions in our series, 13.5% of the malignant effusions, and 24% of the pleural effusions due to mesothelioma.

Although the color of the fluid is a subjective characteristic, the interobserver agreement in our study was fairly good. The differences with some series might be partially explained by the fact that we assessed pleural fluid color in a transparent tube with 10 mL of pleural fluid; the color is usually darker when several hundred milliliters are accumulated.

BPE can also be due to benign diseases. Similar to Light’s experience, the most frequent benign causes in our series were parapneumonic and posttraumatic pleural effusions.1 Coronary artery bypass graft surgery6 and postcardiac injury syndrome7 may frequently produce BPE. One of our patients with internal mammary artery graft surgery had BPE. Pulmonary embolism has been reported to contain a particularly high RBC count.8 In our series, five of eight patients (62%) had either blood-tinged effusions (n = 4; 50%) or BPE (n = 1; 12%). Other less common causes of BPE may be acute aortic dissection,9 thoracic vascular disruption, pancreatitis,10 benign asbestos pleural effusion,11 pseudochylothorax,12 endometriosis,13 lung transplantation,14 esophageal variceal sclerotherapy,15 right-sided endocarditis,16 sarcoidosis,17 hemagiomatosis,18 or intralobar pulmonary sequestration.19

In conclusion, serous and blood tinged were the most common presentations of pleural fluid at thoracentesis. Almost half of BPEs were secondary to neoplasms, but only 11% of the neoplastic effusions were BPE. Other common causes of BPE were parapneumonic and posttraumatic. The appearance of the fluid should not be overemphasized as a diagnostic test.


   Footnotes
 
Abbreviations: BPE = bloody pleural effusion; CI = confidence interval; OR = odds ratio

This study was supported in part by grants C03/011-RTIC from Instituto de Salud Carlos III.

This study has been partially presented at the SEPAR 2002 meeting in Gran Canaria Island, Spain, June 8–11, 2002.

Received for publication February 25, 2003. Accepted for publication July 30, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Light, RW (2001) Pleural diseases. 4th ed. ,42-86 Lippincott, Williams & Wilkins. Philadelphia, PA:
  2. Martesson, G, Petterson, K, Thiringer, G Differentiation between malignant and non-malignant pleural effusion. Eur J Respir Dis 1985;67,326-334[Medline]
  3. Villena, V, López Encuentra, A, Echave-Sustaeta, J, et al Estudio prospectivo de 1000 pacientes consecutivos con derrame pleural: etiología del derrame y características de los pacientes. Arch Bronconeumol 2002;38,21-26[ISI][Medline]
  4. Villena, V, Pérez, V, Pozo, F, et al Amylase levels in pleural effusions: a consecutive unselected series of 841 patients. Chest 2002;121,470-474[Abstract/Free Full Text]
  5. Villena, V, López Encuentra, A, Echave-Sustaeta, J, et al Interferon {gamma} in 388 immunocompromised and immunocompetent patients for diagnosing pleural tuberculosis. Eur Respir J 1996;9,2635-2639[Abstract]
  6. Light, RW Pleural effusions after coronary artery graft surgery. Curr Opin Pulm Med 2002;8,308-311[CrossRef][ISI][Medline]
  7. Stelzner, TJ, King, TE, Antony, VB, et al The pleuropulmonary manifestations of the postcardiac injury syndrome. Chest 1983;84,383-387[Abstract/Free Full Text]
  8. Romero Candeira, S, Hernández Blasco, L, Soler, MJ, et al Biochemical and cytologic characteristics of pleural effusions secondary to pulmonary embolism. Chest 2002;121,465-469[Abstract/Free Full Text]
  9. Hata, N, Tanaka, K, Imaizumi, T, et al Clinical significance of pleural effusion in acute aortic dissection. Chest 2002;121,825-830[Abstract/Free Full Text]
  10. Belfar, HL, Radecki, PD, Friedman, AC, et al Pancreatitis presenting as pleural effusions: computed tomography demonstration of pleural space of pancreatitis exudate. J Comput Tomogr 1987;11,184-187[CrossRef][ISI][Medline]
  11. Hillerdal, G Non-malignant asbestos pleural disease. Thorax 1981;36,669-675[Abstract]
  12. Lee, SS, Trimble, RB Rheumatoid arthritis with bloody and cholesterol pleural effusion. Arch Pathol Lab Med 1985;109,769-771[Medline]
  13. Bhojawala, J, Heller, DS, Cracchiolo, B, et al Endometriosis presenting as bloody pleural effusion and ascites: report of a case and review of the literature. Arch Gynecol Obstet 2000;264,39-41[Medline]
  14. Judson, MA, Handy, JR, Sahn, SA Pleural effusions following lung transplantation: time course, characteristics and clinical implications. Chest 1996;109,1190-1194[Abstract/Free Full Text]
  15. Rajagopalan, N, Hoffstein, V Hemothorax following uncomplicated sclerotherapy for esophageal varices. Chest 1994;106,314-315[Abstract/Free Full Text]
  16. Sexauer, WP, Quezado, Z, Lippman, ML, et al Pleural effusions in right-sided endocarditis: characteristics and pathophysiology. South Med J 1992;85,1176-1180[Medline]
  17. De Vuyst, P, De Troyer, A, Yernault, JC Bloody pleural effusion in a patient with sarcoidosis. Chest 1979;76,607-609[Abstract/Free Full Text]
  18. Hurvitz, CH, Greenberg, SH, Song, CH, et al Hemangiomatosis of the pleura with hemorrhage and disseminate intravascular coagulation. J Pediatr Surg 1982;17,73-75[Medline]
  19. Pratter, MR, Kaemmerlen, JT, Erickson, AD Bloody pleural effusion associated with an intralobar pulmonary sequestration. Chest 1979;75,394-395[Abstract/Free Full Text]




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