J Clin Ultrasound 20:461465, September 1992 0 1992 by John Wiley & Sons, Inc. CCC 0092-2751/92/070461-05 $04.00

Tuberculous Pleural Effusions: Ultrasonic Diagnosis Okan Akhan, MD,* Figen Basaran Demirkazik, MD,* Mustafa N, Ozmen, MD,* Ferhun Balkanci, MD,* Seref Ozkara, MD,P Lutfi Coplu, MD,$ Salih Emri, MD,$ and Aytekin Besim, MD,*

Abstract: Twenty patients with tuberculous pleural effusions were studied with ultrasonography. In 18 patients, ultrasonography demonstrated regular pleural thickening which was less than 1 cm except in 1 case. In 4 cases there were a few pleural nodules, whereas in 2 cases the pleural surface showed small nodularity. The latter finding may be diagnostic for a tuberculous etiology. Eighteen patients had multiple, delicate, mobile septations in the effusions, and a lattice-like appearance had formed in 6 cases. Computed tomography was obtained in 7 cases, and pleural thickening was demonstrated in 6 of them. Ultrasonography is a useful imaging modality in the diagnosis of tuberculous pleurisy. Indexing Words: Tuberculosis, pleural Pleural effusion * Computed tomography X-ray

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Tuberculous pleurisy remains one of the major nonmalignant causes of pleural effusion and should be considered a diagnostic possibility in any patient with an exudative Tuberculous pleurisy is found in about 8% of patients with pulmonary tuberculosis. Although some pleural effusions clear spontaneously, most of the patients will manifest active pulmonary or extrapulmonary tuberculosis within the subsequent 5 years.3 Thus it is important to diagnose tuberculous pleurisy. Investigations of pleural effusions by ultrasonography and computed tomography (CT) play an important role in differentiating from solid masses, demonstrating loculation of fluid, planning thoracentesis, or chest tube placement, but the ability of radiologic studies to reveal the etiology of the fluid accumulation has generally been limited.4 The aim of this study was to determine the ultrasonographic features of tuberculous pleural effusions that might help in predicting a tuberculous etiology. From the Departments of *Radiology and SChest Diseases, Hacettepe University, School of Medicine, and from the tAtatiirk Chest Disease and Surgical Center, Ankara, Turkey. For reprints contact Okan Akhan, MD, Hacettepe University, School of Medicine, Department of Radiology, Hacettepe, 06100 Ankara, Turkey.

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MATERIALS AND METHODS

Twenty patients with tuberculous pleural disease seen in the Hacettepe University Hospital and the Ataturk Chest Disease and Surgical Center in 1990 were included in this study. The ages of the patients were 17 to 57 years with a mean of 30.5 years. Thirteen patients were men and 7 were women. In 12 patients, the pleural effusion was on the right side and in 8 patients on the left side. In all patients, thoracentesis was performed and the pleural fluid was thoroughly analysed. Tuberculous pleurisy was definitely diagnosed in 8 patients by pleural punch biopsy. In those for whom no definite histological diagnosis could be established, the tuberculous etiology was accepted based on the pleural fluid analysis and clinical improvement with anti-tuberculous treatment. There were coexisting parenchymal lesions compatible with tuberculosis seen in the chest X-rays of 7 patients, and in 1 of them sputum culture and smear were positive for acid-fast bacilli. Eleven patients had not received anti-tuberculous treatment at the time of the ultrasound examination, whereas others had been treated for different periods ranging from 8 days to 3 months. Chest ultrasonography was performed using a 461

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Toshiba SSA 90 A scanner with 3.75 MHz convex, 5 MHz sector, and 7.5 MHz linear transducers. Longitudinal, transverse, and oblique scans were obtained using subcostal and intercostal approaches with the patient supine and sitting upright. Although the use of a high-frequency transducer improves resolution, artifactual noise in the near field impairs the recognition of thickening of the chest wall pleura. Therefore the diaphragmatic pleura was examined with particular care for pleural pathology. Thoracic CT with a 9-mm slice thickness was obtained in 7 patients after the ultrasonographic examination. RESULTS

Ultrasonography demonstrated regular thickening of the diaphragmatic pleura throughout the region of fluid in 18 of 20 patients (90%)with tuberculous effusion (Figure 1).The pleural thickening was less echogenic than the diaphragm. Two cases (10%)without pleural thickening had not received anti-tuberculous treatment. In another 9 patients without treatment and also in 3 patients treated for less than 2 weeks, the pleural thickening ranged from 1 mm to 5 mm. The remaining 5 cases, treated for 3 weeks to 7 weeks, had 4 mm to 9 mm pleural thickening. In only 1 patient was the pleural thickness more than 1 cm (13mm). This patient had been receiving treatment for 13 weeks and had minimal effusion.

In addition to basal pleural thickening, 4 patients (20%) had a few nodules over the thickened pleura (Figure 2). Another ultrasonography finding of tuberculous pleurisy was small nodularity of the regularly thickened pleural surface, demonstrated in 2 cases (10%)(Figure 3). In total, 6 patients had pleural nodules. We found multiple delicate, complete septations and incomplete fibrils attached to the parietal and visceral pleuras in effusions of 18 cases (90%) (Figure 4). The bands were floating with respiratory movement and transmitted pulsation of the heart. In 6 cases (30%)the septations had formed a lattice-like appearance (Figure 5). In 3 of these cases the patients had been having treatment and had a more complicated meshwork than those without treatment (Figure 6). We examined one of the patients twice-before and 2 months after beginning treatment. At first, he had a few floating bands and a 3-mm pleural thickening. In the second examination, he still had pleural effusion, but a meshwork of bands had formed and the pleural thickening had increased to 6 mm. CT revealed regular pleural thickening in 6 patients with tuberculous pleurisy (Figure 7A, B). DISCUSSION

Pleural effusions in tuberculosis occur when a subpleural focus of parenchymal tuberculosis ruptures into the pleural surface.2 Many experimental studies have shown that introduction of

FIGURE 1. Real-time ultrasonography demonstrates pleural effusion (EFF) and a thin (3 mm), regular pleural thickening in tuberculous pleurisy (D: diaphragm).

FIGURE 2. Right thoracic ultrasonography reveals pleural effusion, pleural nodule (arrowheads), and pleural thickening (2 mm). JOURNAL OF CLINICAL ULTRASOUND

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F\GUR€ 3. Longitudinal real-time ultrasonography demonstrates pleural effusion (p) and diffuse small nodularity of pleural surface (arrows) in tubeculous pleurisy (D: diaphragm; S: spleen).

FIGURE 4. Longitudinal view shows pleural effusion (PI, regular pleural thickening (arrows), and thin septations (arrowheads).

tuberculin protein into the pleural cavity results in a vigorous outpouring of serous exudate; in sensitized animals, well-organized granulomata were shown on the pleural surface at 10 days.5 Pleural effusions may also result from hematogenous dissemination of mycobacteria and by direct extension of primary disease.2 Although tuberculous pleuritis usually re-

solves spontaneously, treatment is necessary to prevent the subsequent development of some active form of tuberculosis (pulmonary or extrapulmonary), to relieve the patient’s symptoms, and to prevent the development of a fibrothorax. Even if the pleura has been thickened when the patient’s disorder is first diagnosed, the thickness may decrease with treatment within 6

FIGURE 5. A lattice-like appearance is shown in the effusion of tuberculous pleurisy.

FIGURE 6. Left thoracic longitudinal ultrasonography demonstrates a meshwork of fibrils in pleural effusion and pleural thickening 16 diaphragm). mm), (0:

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FIGURE 7. (A) Thoracic CT reveals regular pleural thickening (arrowheads) and pleural effusion in tuberculous pleurisy. (B) In the same patient, chest ultrasonography demonstrates thin septations (arrows) in tuberculous pleural effusion (P EFF) and pleural thickening (D:diaphragm; S: spleen).

months.6 Therefore, it is important to diagnose the tuberculous etiology and follow up the amount of effusion and pleural thickening occurring during treatment. Thin, complete and incomplete, mobile bands with or without a lattice-like appearance in pleural effusions, regular pleural thickening and small nodularity of pleural surface should arouse the suspicion of a tuberculous etiology for a pleural effusion. Although in 1989 Martinez et al. reported winding, bands and linear echoes in tuberculous pleurisy, they did not mention pleural thickening and the lattice-like a p p e a r a n ~ eIn . ~ the literature, pleural thickening has been demonstrated ultrasonographically in a few cases of tuberculous pleurisy.8 The time of the first examination after the appearance of pleural effusion may influence the ultrasonography findings. We observed in 1 case that the pleural fluid became more complex and the pleural thickening increased during the course of followup. The parietal pleura was not seen in 2 cases, and in other cases the pleura seemed to get thicker with time. CT also demonstrated thin, regular pleural thickening in 6 of 7 cases, consistent with the reports of other author^^,'^^^^; but it failed to demonstrate the thin septations. A lattice-like appearance and smooth pleural thickening can be detected in association with empyemas and hemothoraces by ultrasonography.8,'2,'3 In this situation, the correct diagnosis

may be made only by pleural fluid analysis taken under ultrasonographic guidance when necessary. Metastatic carcinoma and mesothelioma should also be considered in the differential diagnosis of tuberculous pleurisy. Thoracoscopic studies in malignant pleural lesions have shown different cancer patterns: (a) nodules or masses easily distinguished from fibrinous clots, (b) pleural thickening, (c) pleural thickening mixed with sessile masses or nodules on the surface of large, thick cancerous plaques, (d) lymphangitis, and (e) nonspecific changes.14 In inflammatory conditions, different thoracoscopic findings ranging from hyperemia to opalescent, shiny thickening may be detected. Tuberculous pleurisy is characterized by small, white-gray nodules over the pleural surface with or without inflammatory change.l4>l5 Because of this, ultrasonographic detection of large, confluent pleural masses and irregular, sheet-like pleural thickening and thick bands with decreased motility are indicative of mesothelioma and metastatic carcinoma.8,17J8

CT of pleural pathologies have also demonstrated that focal pleural masses or thick irregular pleurae are consistently associated with malignancies.l07l1Leung et al. reported a specificity of 94% and a sensitivity of 36%for CT detection of parietal pleural thickening greater than 1cm, and a sensitivity of 94% and a specificity of 54% for nodular pleural thickening. JOURNAL

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We agree that pleural thickness is a valuable parameter in the differential diagnosis, as all of our cases except one showed regular pleural thickening less than 1 cm. Although Fataar has detected pleural thickening up to 20 mm in 10 patients with empyema and 2 with tuberculous pleurisy by ultrasonography,8 pleural thickening of more than 1 cm should arouse the suspicion of malignancy if it is detected at the time of the initial diagnosis of the patient’s disorder. We found a few nodules over regular pleural thickening in 4 patients. This shows that focal pleural nodularity does not always indicate a malignant pathology and could be seen with fibrothorax.ll Ultrasonography demonstrated diffuse small nodularity of the surface of regularly thickened pleurae that may be the ultrasonographic appearance of granulomas in 2 cases. However, in 1 of them, biopsy was not diagnostic, whereas in the other patient biopsy revealed many granulomas with caseification in fibrous tissue. In our opinion, diffuse small nodularity of a pleural surface seen by ultrasonography may be a diagnostic feature of tuberculous eti01ogy.l~ We conclude that the ultrasonographic findings of thin, regular pleural thickening; mobile, complete and incomplete septations that may form a lattice-like appearance; and diffuse, small nodularity of the pleural surface are strongly suggestive of tuberculous pleurisy as in tuberculous p e r i t o n i t i ~ However, . ~ ~ ~ ~ ~a definite diagnosis should be made by thoracentesis and other procedures. In addition, the value of ultrasonography in following the response of patients to anti-tuberculous treatment by repeatedly demonstrating the amount of fluid and pleural thickness should be investigated.

REFERENCES 1. Herbert A: Pathogenesis of pleurisy, pleural fibrosis and mesothelial proliferation. Thorax 41:176189,1986. 2. Steven AS: The pleura. Am Reu Respir Dis 138:184-234, 1988. 3. Brason FW: Tuberculous pleural effusion, in Brason FW: Pleural Effusion, Mount Kisco, New York, Futura Publishing, 1986, p 211.

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4. Sheila DD, Henschke GI, Yankelevitz DF, et al: MR imaging of pleural effusions. J Comput Assist Tomogr 14:192-198, 1990. 5. Antony VB, Repine JE, Harada RN, et al: Inflammatory responses in experimental tuberculosis pleurisy. Acta Cytologica 27:355-361, 1983. 6. Light RW: Tuberculous pleural effusions, in Light RW: Pleural Diseases, Philadelphia, Lea & Febiger, 1983, p 123. 7. Martinez OC, Serrano BV, Romero RR: Real-time ultrasound evaluation of tuberculous pleural effusions. J Clin Ultrasound 17:407-410, 1989. 8. Fataar S: Ultrasound in chest disease: 1. Pleura. Australas Radiol 32:295-301, 1988. 9. Hulnick DH, Naidich DP, McCauley DI: Pleural tuberculosis evaluated by computed tomography. Radiology. 149:759-765, 1983. 10. Maffessanti M, Tommasi M, Pellegrini P: Computed tomography of free pleural effusions. Europ J Radiol 7:87-90, 1987. 11. Leung AN, Muller NL, Miller RR: CT in differential diagnosis of diffuse pleural disease. A J R 154~487-492,1990. 12. Goldenberg NJ, Spitz HB, Mitchell SE: Gray scale ultrasonography of the chest. Seminars in Ultrasound 3:263-277, 1982. 13. Hirch JH, Carter SJ,Chikos PM, et al: Ultrasonic evaluation of radiographic opacities of the chest. A J R 130~1153-1156,1978. 14. Boutin C, Viallat JR, Cargnino P, e t al: Thoracoscopy in malignant pleural effusions. Am Reu Respir Dis 124:588-592, 1981. 15. Canto A, Blasco E, Casillas M, et al: Thoracoscopy in the diagnosis of pleural effusion. Thorax 32~550-554, 1977. 16. Boushy SF, North LB, Helgason AH: Thoracoscopy: Technique and results in eighteen patients with pleural effusion. Chest 74~386-389, 1978. 17. Miller JH, Reid BS, Kemberling R: Water-path ultrasound of chest disease in childhood. Radiology 152~401-408,1984. 18. Goerg C, Schwerk WB, Goerg K, et al: Pleural effusion: An “acustic window” for sonography of pleural metastases. J Clin Ultrasound 19:93-97, 1991. 19. Akhan 0, Demirkazik FB, Demirkazik A, et al: Tuberculous peritonitis: ultrasonic diagnosis. J Clin Ultrasound 18:711-714, 1990. 20. Gompels BM, Darlington L G Ultrasonic diagnosis of tuberculosis peritonitis. B r J Radiol 51:10181019,1978.

Tuberculous pleural effusions: ultrasonic diagnosis.

Twenty patients with tuberculous pleural effusions were studied with ultrasonography. In 18 patients, ultrasonography demonstrated regular pleural thi...
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