(Chest. 2004;125:1776-1782.)
© 2004
American College of Chest Physicians
Percutaneous Multiple-Site Parietal Pleural Biopsy*
Description and Evaluation of a New and Safe Technique
Babu Uthaman, DM;
Nasser Behbehani, BMBCh;
Adnan Abal, BMBCh;
John Madda, MBChB and
Siddiq Khan, MD
* From the Department of Medicine (Drs. Uthaman, Behbehani, and Abal), Faculty of Medicine, Kuwait University, Safat, Kuwait; the Microbiology Department (Dr. Khan), Chest Diseases Hospital, Kuwait City, Kuwait; and the Pathology Department (Dr. Madda), Amiri Hospital, Kuwait City, Kuwait.
Correspondence to: Babu Uthaman, DM, Department of Medicine, Faculty of Medicine, Kuwait University, PO box 24923, 13110 Safat, Kuwait; e-mail: bsuthaman{at}hotmail.com
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Abstract
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Study objectives: (1) To describe a new percutaneous pleural biopsy technique to obtain multiple-site parietal pleural biopsy specimens in patients with pleural effusion (PE), and (2) to evaluate its effectiveness and safety compared to current techniques.
Design: Prospective interventional study.
Setting: University teaching hospital.
Patients: Consecutively referred for evaluation of exudative PE.
Intervention: With the patient in a semirecumbent position, a 9F sheath was inserted by the Seldinger technique into the pleural cavity on the midaxillary line under local anesthesia and fluoroscopic guidance. An 8F bioptome was introduced through it, and biopsy specimens were taken from several sites on the costal and diaphragmatic pleura. After biopsy, PE was completely evacuated, and the sheath was removed.
Results: During the 2-year pilot study, we procured, on average, 14 adequate pleural specimens from each of the 28 patients (age range, 15 to 81 years) on the first attempt. Histopathologic examination revealed tuberculous pleuritis (18 patients), metastatic adenocarcinoma (1 patient), and nonspecific pleuritis (9 patients). Postprocedure, 25 patients had rapid symptomatic improvement without recurrence of PE. No major complications occurred during or after the procedure (mean follow-up period, 2 years).
Conclusions: Our new biopsy procedure can be performed easily, safely, and with increased diagnostic sensitivity and patient comfort. Unlike other biopsy techniques, it provides adequate multiple-site pleural biopsy specimens, in all cases, on the first attempt without any morbidity and mortality. It has a therapeutic potential to provide rapid symptomatic relief and treatment by pleurodesis. We recommend this procedure for patients whose conditions remain undiagnosed after undergoing needle biopsy or for those who cannot tolerate it, before considering more aggressive diagnostic interventions. This is the best alternative when thoracoscopy or thoracotomy are not available or when patients are at high risk for complications from them.
Key Words: bioptome • granuloma • histopathology • malignant • parietal pleural biopsy • percutaneous pleural biopsy • pleural effusion • pleuritis • tuberculous
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Introduction
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Needle biopsy of the pleura is a routine invasive investigation in the etiologic diagnosis of exudative pleural effusion (PE).123 The diagnostic accuracy of the needle biopsy, however, is limited because it procures pleural tissues from around a single puncture site. Studies45 have shown that in 23 to 28% of patients PE remains etiologically undiagnosed, despite relevant investigations including thoracentesis and needle biopsy. Thoracoscopy and thoracotomy are the ultimate diagnostic options.67 These are specialized procedures that are associated with certain complications and discomfort to the patient. Earlier, we introduced a percutaneous technique using a bioptome for multiple-site biopsies of the parietal pericardium.89 Drawing on that experience, we developed a new percutaneous pleural biopsy technique that yields better results than needle biopsy, and is simpler than thoracoscopy and thoracotomy. This article describes our technique, and prospectively evaluates it in terms of its effectiveness, safety, and complications, compared to published reports of pleural biopsy techniques by needle, thoracoscopy, and thoracotomy.
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Materials and Methods
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During the 2-year pilot study, 28 patients in whom exudative PE was diagnosed by clinical, radiologic, and initial pleural fluid examination were selected for the procedure. Informed consent was obtained from all patients. Six of these patients had undergone unsuccessful attempts at biopsy using an Abrams needle earlier. Four patients could not tolerate the procedure, and in the other two patients sufficient pleura could not be obtained. There were 19 men and 9 women ranging in age from 15 to 81 years (mean age, 39 years). They had been symptomatic for periods ranging from 1 week to 6 months.
Biopsy Technique
The procedure is performed in the cardiac catheterization laboratory with the patient lying in a semi-recumbent position, and premedicated with morphine and promethazine hydrochloride. After local anesthesia with lidocaine was administered, a long 18-gauge needle attached to a syringe filled with lidocaine was inserted into an intercostal space below the fluid level (generally the sixth to eighth space) on the midaxillary line along the upper border of the lower rib. The needle is advanced slowly, periodically attempting to aspirate fluid and then injecting a small amount of lidocaine to clear the needle and to anesthetize the deeper tissues. The entry to the pleural space is indicated by a sensation of "giving way" and the aspiration of fluid. With the needle held stationary, the syringe is disconnected and the soft end of a 0.038-inch J-tip guidewire (GW) is inserted through the needle to the pleural cavity. It is advanced under fluoroscopic guidance until it touches the mediastinum and becomes curved in the cavity (Fig 1 ). Further feeding of the GW will deflect it either laterally, to face the costal surface, or inferiorly, to face the diaphragmatic surface of the parietal pleura. The needle is removed, and a small incision is made with an 11 blade at the entry site along the GW. The entry path is predilated with a 10F dilator. A 9F long sheath reinforced with a dilator (Mullins Transeptal Check-Flo Introducer Set; Cook; Bjaeverskov, Denmark) [Fig 2
] then is passed over the GW until it reaches the costal or diaphragmatic pleura. The long sheath should have a curved tip, to facilitate a change of direction during manipulations, and a hemostatic valve, to prevent pneumothorax and pleural fluid leak during the procedure. The dilator and GW are withdrawn, and sufficient fluid is aspirated for relevant investigations.
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Figure 1. Cine frames showing (top left, A) the GW introduced through the puncturing needle into the pleural cavity, (top right, B) the long sheath passed over the GW into the pleural cavity, (middle left, C) the bioptome introduced through the long sheath into the pleural cavity, (middle right, D) the bioptome advanced through the sheath to the diaphragmatic pleura, (bottom left, E) the bioptome directed to the lateral costal pleura for biopsy, and (bottom right, F) the bioptome manipulated to the posterior costal pleura for biopsy.
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Figure 2. The instruments used for multiple parietal pleural biopsies are shown, as follows: (A) the long dilator used to reinforce the long sheath for entry to the pleural cavity through the chest wall; (B) the bioptome with the jaws on the left side, and the handle to open and close the jaws over the right side; (C) the long sheath with curved tip and the hemostatic valve for inserting the bioptome into the pleural cavity; and (D) the magnified picture (inset) of the jaws of the bioptome in the open position.
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An 8F bioptome with large serrated jaws (RadialJaw 3 biopsy forceps with needle; Boston Scientific Microvasive; Watertown, MA) [Fig 2] then is advanced through the long sheath until the jaws protrude from it. With the jaws open, the bioptome is advanced further and applied to the parietal pleura. The biopsy sample is taken by closing the jaws and withdrawing the bioptome from the sheath. The sheath then is manipulated to direct its tip to other areas of the costal and diaphragmatic pleura for further biopsy. During manipulation, the sheath should be reinforced with a catheter, dilator or bioptome both to provide torque for manipulations and to prevent kinking of the thin-walled sheath. To position the sheath in an entirely different area (for example, from the diaphragmatic to the costal surface), it is reinforced by the long dilator. The GW is reinserted, manipulated, and advanced to the target area with the help of the sheath and dilator. The sheath is then slid over the GW to the target area for taking the biopsy specimen. In this manner, multiple biopsy specimens can be taken from several sites on the costal and diaphragmatic pleural surfaces (Fig 1). Biopsy specimens are not taken from the mediastinal surface to avoid injury to the heart and other vital structures. The entire procedure is performed under fluoroscopic guidance, while monitoring the ECG and oxygen saturation.
After adequate biopsy specimens are procured, a pigtail catheter is inserted through the sheath to the pleural cavity to aspirate all of the fluid and an occasional small amount of air that is inadvertently introduced during repeated passage of the bioptome. After complete evacuation, the sheath and catheter are pulled out while applying continuous suction to the catheter with a syringe to remove the last drop of air and fluid on the way out. Pinching the skin and subcutaneous tissue around the catheter at the entry site will prevent pneumothorax from occurring during and after catheter removal. The wound is sealed with antibiotic cream and elastocrepe bandage. The patient is kept under observation for 24 h. The biopsy material is sent for histopathologic and mycobacterial investigations.
Massive PE can present two problems. First, the bioptome tends to slip away from the pleural surface during the bite because of the "roomy" pleural space, and the inherent flexibility of the bioptome and sheath. The partial evacuation of fluid before inserting the bioptome reduces the pleural space. This restricts free movement of the bioptome and helps to anchor it to the pleural surface for the bite. Second, rapid complete aspiration of a massive PE may produce reexpansion pulmonary edema. In such cases, the sheath is removed over the GW, and a pigtail catheter is inserted over it to the pleural cavity for continued drainage until the fluid ceases to accumulate.
Obesity and overcrowding of the ribs may make it difficult to palpate and localize the intercostal space to insert the relatively thick biopsy needle. In such patients, we palpate the rib and puncture the skin with the sharp needle, aiming at the upper border of the rib. Once the rib is struck, the needle (with the skin and subcutaneous tissue) is slid over the upper border of the rib and is inserted easily through intercostal muscles to the pleural cavity.
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Results
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Fourteen patients had PE over the right side and an equal number over the left side. On average, 919 mL pleural fluid was aspirated during the procedure (range, 2 to 2,500 mL). We procured multiple pleural tissue specimens from multiple areas of the parietal pleura in all 28 patients on the first attempt. The number of pleural biopsy specimens ranged from 10 to 18, with an average of 14. Comparison by the pathologist revealed that our biopsy procedure procured, on an average, approximately five times more volume of pleura than the needle biopsy procedure, and all specimens contained pleural tissue. The bioptome induced minimal tissue distortion while providing similar depth of pleura as the biopsy needle. Six patients with > 1,500 mL PE required the partial removal of fluid to anchor the bioptome to the pleural surface for the bite. Biopsy material was adequate to yield histopathologic diagnoses in all 28 cases (Table 1
).
There were no major complications during the procedure. Patients tended to have cough and pain toward the end of complete aspiration, and while the catheter was being pulled out. One patient had localized subcutaneous emphysema at the puncture site. In three patients, despite the presence of the hemostatic valve, repeated passage of the bioptome introduced air bubbles through the sheath to the pleural cavity. The fluid and air were completely evacuated during catheter removal at the end of the procedure.
The catheter was withdrawn from the pleural cavity immediately after biopsy and complete aspiration in all except two patients. In these two cases (with malignancy and liver cirrhosis), the catheter was retained in the pleural space for further aspirations due to large residual PE, even after the removal of 2,500 mL hemorrhagic fluid. The patient with malignant PE pneumothorax 2 days postprocedure required chest tube drainage for a week. The cirrhotic patient needed catheter drainage for 2 weeks before complete resolution. Of the 26 patients who had the catheter removed soon after the procedure, fluid reaccumulated in only one patient. Although the initial results of testing of his biopsy specimen showed nonspecific pleuritis, he required repeated thoracentesis, and 2.5 months later thoracoscopy revealed extensive infiltration of visceral and parietal pleura by non-Hodgkin lymphoma. PE did not recur in the remaining 25 patients.
Follow-up
All 28 patients were followed up for an average period of 2 years (range, 6 months to 4 years) [Table 2
]. No patients had complications related to the biopsy procedure. Of the nine patients with nonspecific pleuritis revealed by biopsy, one turned out to have non-Hodgkin lymphoma. Another patient had oat cell carcinoma of the bronchus, which was diagnosed by fine needle aspiration of a concomitant mediastinal mass. The rest, followed up for an average period of 3.7 years (range, 3 to 4 years), had complete resolution of PE without further recurrence. None showed evidence of tuberculosis or malignancy on follow-up. Hence, we think that we could identify all 18 cases of tuberculous PE in this cohort by biopsy-proven diagnosis of granuloma.
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Discussion
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Even after several modifications of needle design and biopsy procedures, the needle biopsy technique continues to have several limitations and complications, which our biopsy technique attempts to address and eliminate.10 Pleural tissue may be absent from the needle biopsy specimen, or it may be inadequate or unsuitable for proper diagnosis in about 2 to 14% of cases.51112 This necessitates the performance of two or more repeat biopsies in 
15.5% of patients.4 Studies61314 have shown that obtaining multiple samples from a single site by needle biopsy and larger pieces from multiple sites by thoracoscopy increased the diagnostic sensitivity for both tuberculosis and malignancy. Our procedure provides multiple biopsy specimens from multiple sites of the parietal pleura, thus offering a histopathologic diagnosis in all cases on the first attempt. As the bioptome is directly applied to the parietal pleura, all biopsy samples contain pleural tissue larger than the thin strip of the pleura obtained by the needle. This is because the bioptome "plucks" the pleura directly while the needle cuts it with underlying tissues. At times, the bioptome plucks pleural samples that are considerably larger than the size of the biopsy cup, especially when the pleura is inflamed and fleshy. Occasionally, it peels off a sheet of pleura, which can be taken out through the long sheath intact. Our experience indicates that it is difficult, if not impossible, to take biopsy specimens from a normal pleura and that the specimen obtained is likely to be small.
Our biopsy technique offers several safety features and advantages that are not seen with the needle biopsy technique. Insertion of a soft J-tipped GW as soon as fluid is struck ensures atraumatic entry to the pleural cavity. It also prevents the sharp puncturing needle from traumatizing the lung and adjoining viscera, even in the presence of a small PE. The sheath facilitates the repeated insertion of the bioptome to the pleural space for multiple biopsies without any discomfort. It also protects the lung and vascular structures in the costal groove, thereby decreasing the chance for pneumothorax and hemothorax. The biopsy of extrapleural tissues occurred in 0.8% of cases during the needle biopsy, the incidence being higher (16%) with minimal fluid.312 The sheath directs the bioptome away from the lung during the biopsy. The blunt end of the bioptome and its manipulations under fluoroscopic guidance prevent transdiaphragmatic entry to the abdomen. All these factors help to avoid the biopsy of extrapleural tissues. The sheath also helps to direct the bioptome to several sites of the pleura for multiple biopsies. Our technique can be performed successfully even with small or loculated PEs, provided there is sufficient fluid (which is an "absolute prerequisite") to allow safe needle entry followed by GW insertion into the pleural cavity. We had two patients with loculated PE who had 2 mL and 140 mL of fluid, respectively. In the first patient, a thickened pleura with minimal fluid gave the misleading chest radiograph appearance of moderate PE. In this patient, we introduced the GW as soon as the needle struck fluid (in the second puncture at a different site, as the first puncture did not yield fluid). The GW and sheath dilator unit could be manipulated through the adhesions to procure multiple-site biopsy specimens. Postprocedure aspiration yielded only 2 mL of fluid, indicating an essentially dry pleural space. We would not have introduced the GW if fluid had not been struck, and we could not have performed the biopsy if the sheath could not be inserted over the GW to the pleural space. In both these cases, we obtained multiple biopsy specimens without complications. This would be difficult and even hazardous to do with the needle biopsy technique, which requires moderate PE to avoid complications.12
Needle biopsy of the pleura is usually performed with the patient in a sitting position, resting the arms and head on an overbed tray. For a sick or obese patient, this may not be a comfortable position to tolerate the insertion of the thick biopsy needle several times through the chest wall. Our biopsy procedure is performed with the patient well-sedated in a comfortable semi-recumbent position on a table with the arms supported above the head. This position allows the fluid to gravitate to the lower part of the pleural cavity around the lung at the needle puncture site to minimize the occurrence of potential complications. Elevating the hands above the head widens the intercostal space for safe entry into the pleural cavity. This technique enabled us to obtain multiple biopsy specimens easily in three patients who were too sick to sit up and cooperate during a previous needle biopsy procedure. Using our modified technique, we also could enter the pleural space safely and take 18 biopsy specimens in an ill 81-year-old woman, in whom obesity and overcrowding of the ribs made it impossible to palpate the intercostal spaces to pass the Abrams needle in an earlier attempt.
We did not encounter any immediate or late complications, which have been reported in 15% of needle biopsy procedures.35 The delayed pneumothorax in the patient with massive malignant PE did not appear to have been caused by our procedure. The use of the catheter and long sheath with hemostatic valve allows the complete evacuation of both fluid and air from the pleural cavity after the procedure, without traumatizing the lung. This is not possible with the conventional needle biopsy technique. It has been shown15 that the initial complete drainage of the PE after thoracoscopy gave greater symptomatic improvement than any subsequent therapy. We also noted rapid symptomatic relief in all cases with complete evacuation and no further reaccumulation. Thus, our biopsy procedure proved to have a therapeutic potential in 25 of 28 cases (89%), in addition to its diagnostic capability. This therapeutic effect was noted in both nonspecific and tuberculous PEs.
The rapid diagnosis of tuberculous PE can be made by demonstrating the occurrence of granuloma in a needle biopsy specimen of the pleura in 50 to 80% of cases.16 In comparison, our technique, by obtaining multiple biopsy specimens from several sites, could demonstrate granuloma in all 18 cases (100%) of tuberculous PE. This result is even better than those obtained by thoracoscopy (94%).17 PEs associated with malignancy may result from invasion of the pleura by neoplastic disease (direct extension or metastasis) or can occur without actual invasion (local or systemic effects of the tumor or its ther-apy).517 In these paramalignant effusions, the results of testing the pleural biopsy specimen will remain negative until the pleura is infiltrated by malignancy. Hence, a 100% diagnostic sensitivity cannot be expected in malignancy-associated PE, as was shown by two of our patients (those with oat cell carcinoma and non-Hodgkin lymphoma). Thoracoscopic and autopsy studies1819 of pleural metastasis have shown localized lesions to be inaccessible to needle biopsy in 32 to 47% of cases. Thoracoscopy also has demonstrated the nonuniform location of pleural metastases (84% in the lower portions of the hemithora-ces on the diaphragmatic, costal, and mediastinal pleura).18 Therefore, our technique, by obtaining multiple-site biopsy specimens from the lower costal and diaphragmatic pleura, is more likely to pick up such patchy malignant pleural involvement than is the needle biopsy from a single point on the costal pleura. Also, large samples with minimal tissue distortion that were gathered by our method may characterize the type and origin of malignancy better than cytology and needle biopsy.1117
Thoracoscopy, using a rigid thoracoscope or newer semiflexible thoracofiberscope, allows visually guided multiple biopsies of abnormal pleura, thereby yielding better results.620 It is indicated if the cause of PE remains undiagnosed after the needle biopsy procedure. Thoracoscopy helps to stage malignancy, to perform pleurodesis, and to provide rapid symptomatic recovery due to complete drainage.1517 Thoracoscopy can be performed under sedation and local anesthesia by trained pulmonologists, but requires special instruments and the induction of pneumothorax.1720 Currently, the expertise and newer instruments are not widely available, and semiflexible thoracofiberscopes provide only small biopsy specimens.20 Thoracotomy (ie, surgical exposure under general anesthesia) provides the best biopsy sample and is indicated only in patients with progressive, otherwise undiagnosed PE.7 Both thoracoscopy and thoracotomy require chest tube drainage for lung expansion and are associated with complications, particularly in sick patients.61721 Compared to needle biopsy, their additional contributions to the diagnostic sensitivity, however, is limited, and an etiologic diagnosis may remain elusive despite these investigations.72021 Short of direct visualization, our biopsy procedure also can provide multiple large biopsy specimens from several sites, thereby offering similar diagnostic sensitivity as these specialized procedures. It too provides rapid symptomatic recovery and treatment with pleurodesis. However, some additional advantages are that it is less expensive, less invasive, and less complicated to perform than both thoracoscopy and thoracotomy, and it can be performed safely even in very sick and obese patients.
The limitation of our technique is that it is a blind biopsy procedure and cannot be performed at bedside. It requires facilities for fluoroscopy, and instruments like GW, sheath, catheter, and bioptome along with the skill to handle them. But these are available in most hospitals caring for patients with PEs.
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Conclusions
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We conclude that our new pleural biopsy technique can offer many safety features and can overcome many of the limitations of the conventional needle biopsy procedures. Our technique increases the diagnostic sensitivity by providing multiple biopsy specimens of the parietal pleura that are inaccessible to the biopsy needle. With the exception of thoracoscopy and thoracotomy, this is the only biopsy technique described so far that has been uniformly successful in procuring adequate pleural tissue specimens in all cases, on the first attempt, without any morbidity and mortality. Yet, it is simpler and less traumatic than thoracoscopy and thoracotomy, and can be carried out easily and safely, even in sick and obese patients. Apart from its diagnostic capabilities, it has therapeutic potential. We recommend this procedure for patients in whom PE remains undiagnosed after the needle biopsy or in those who cannot tolerate it, before subjecting them to thoracoscopy or thoracotomy. This is the best alternative when these specialized procedures are not available or when patients are at high risk for complications from them.
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Footnotes
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Abbreviations: GW = guidewire; PE = pleural effusion
Received for publication January 30, 2003.
Accepted for publication October 17, 2003.
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References
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Abstract
Introduction
