ORIGINAL ARTICLES
Percutaneous Transthoracic Aspiration Needle Biopsy Stuart S. Sagel, M.D., Thomas B. Ferguson, M.D., John V. Forrest, M.D., Charles L. Roper, M.D., Clarence S. Weldon, M.D., and Richard E. Clark, M.D: ABSTRACT An experience based on 1,211 patients has shown aspiration needle biopsy to be a valuable technique for diagnosing bronchogenic carcinoma and other localized intrathoracic lesions that are beyond the reach of the fiberoptic bronchoscope.In 896 patients with malignant intrathoracic neoplasm, the aspirate demonstrated malignant cells in 96%. A false cytological diagnosis of carcinoma occurred in 2 patients, for a true positive rate of 99%. However, the true negative rate was only 87%. In 77% of 31 immunosuppressed patients, the causative agent of a focal infectious process was diagnosed. Pneumothorax was the only notable complication, occurring in 24% of patients, with 14% requiring chest tube drainage. The procedure is relatively simple and rapid, generally causes little patient discomfort, and can be performed in virtually any hospital.
While the chest radiograph is a sensitive method for detecting pulmonary pathology, it usually lacks the specificity required for etiological diagnosis and treatment planning. The determination of the cause of a pulmonary nodule, mass, or focal infiltrate remains a common clinical problem generally requiring cytological, histological, or microbiological studies. Percutaneous lung puncture has been used as a diagnostic technique since the late nineteenth century, but the lack of adequate visual control and proper equipment can lead to major complications. During the last decade, interest in the contribution of percutaneous aspiration needle biopsy has been accelerated by the high degree of diagnostic accuracy made possible by television-monitored fluoroscopy, improved needles, and advanced cytoFrom the Mallinckrodt Institute of Radiology, and the Division of Cardiothoracic Surgery, Washington University School of Medicine, St. Louis, MO. Presented at the Fourteenth Annual Meeting of The Society of Thoracic Surgeons, Jan 23-25, 1978, Orlando, FL. Address reprint requests to Dr. Sagel, 510 S Kingshighway Blvd, St. Louis, MO 63110.
399 0003497517810026-0503$01.25 @ 1978 by Stuart S. Sagel
pathological techniques [ 2 ] . The failure of this procedure to spread widely, especially to nonuniversity hospitals, has been discouraging to its proponents. Our purpose is to emphasize the simplicity, rapidity, safety, and high diagnostic accuracy of the technique.
Materials and Method During the past 5% years, 1,211 patients, ranging from 15 to 91 years old, have undergone percutaneous transthoracic aspiration needle, biopsy at the Mallinckrodt Institute of Radiology. The overwhelming majority of patients were referred for consultation from the Division of Cardiothoracic Surgery and the Pulmonary Medicine Service of Barnes Hospital when the cause of a persistent localized pulmonary mass or infiltrate remained undiagnosed by conventional modalities, such as sputum examination and culture, bronchoscopy, and serological studies. The complete technique of pulmonary aspiration needle biopsy has been described in detail previously [lo] and will be only summarized here. That the procedure is easily learned and accomplished, rarely takes longer than fifteen minutes to perform, and requires no complex equipment or devices deserves emphasis. Testing for a bleeding diathesis is done by a coagulation laboratory survey in the cachectic cancer suspect or the immunosuppressed patient before proceeding with the biopsy. Premedication is usually unnecessary. If the patient is particularly apprehensive despite reassurance given while obtaining informed consent, Valium (diazepam) is administered before aspiration. In patients with severe pain before biopsy (e.g., those with a tumor of the superior sulcus), use of narcotic analgesia facilitates performance of the procedure. Following localization of the lesion by chest radiography and fluoroscopy, the patient is placed on a fluoroscopic table in the position that permits the most direct needle access. In
400 The Annals of Thoracic Surgery Vol 26
No 5 November 1978
general, this is either the supine or prone position. With a lesion near the lateral chest wall, the patient may be placed in a lateral decubitus position; and with a lesion located just above the hemidiaphragm, a rare finding, an upright attitude is used. Under fluoroscopic control, a point on the skin, usually one directly overlying the lesion, is marked. The patient’s skin is cleansed, the puncture site is infiltrated with local anesthesia, and a small skin and subcutaneous tissue stab incision is made with a scalpel blade before the needle is introduced. With intermittent fluoroscopy to aid straight passage, the tip of the aspirating needle is advanced to the appropriate depth. This is gauged either by estimation from previous chest radiographs or tomograms or both, or by inserting the tip until a change in consistency of the lung is felt. The relationship between the needle tip and the lesion is monitored by having the patient breathe shallowly. Sometimes it is necessary to turn the patient slightly to better ascertain that the needle tip abuts the lesion. A television-monitored single-plane image intensification fluoroscopy (preferably with an over-the-table tube) is required. Such readily available equipment almost always suffices for needle localization. We generally use an 18-gauge Turnermodified aspirating needle [17].* The sharp outer cannula of this needle permits larger fragments of tissue to be obtained than do similar gauge spinal needles. Harvest of these tissue fragments increases the incidence of specific histological diagnosis over cytological techniques alone. With the needle tip positioned adjacent to the lesion, the internal stylet is removed, and a 10-ml syringe is quickly attached to the needle hub. With the application of continuous suction, the needle tip is moved back and forth over a 0.5- to 1.0-cm distance several times, using a jabbing and rotating motion through the lesion. Then the needle is withdrawn. Suction is released and the aspirated material is flushed into a sterile balanced electrolyte solution (Polysal). If a small core of tissue is identified, it is transferred to 10% formalin solution for subsequent histological *Available from Cook, Inc, Bloomington, IN 47401.
study. The number of lung punctures is variable, usually ranging from 1 to 5 per patient. The procedure is repeated as many times as necessary until small tissue fragments can be seen in the solution. This material is sent for appropriate pathological (cytology and cell block) or microbiological studies or both. After the biopsy procedure, a frontal upright expiration chest radiograph is made to evaluate for a complicating pneumothorax. If pulmonary neoplasm is suspected and if the samples from the initial procedure are negative, a second biopsy procedure is performed, either the same day or the following morning. An attempt is made to sample from different parts of the lesion. If no malignant cells are detected on only one biopsy attempt in patients in whom the suspicion of carcinoma is high, the study should be considered technically incomplete. If a pneumothorax occurs after the first biopsy procedure, a chest tube is inserted before the procedure is repeated. The presence of the chest tube permits aggressive sampling on the second biopsy since the major potential complication of pneumothorax has been removed.
Results Diagnostic Accuracy Aspiration needle biopsy of a localized intrathoracic mass or infiltrate was performed in 1,153 patients in whom cancer was a clinical consideration. Of these patients, 896 had a malignant intrathoracic neoplasm as evidenced by either surgical proof or postmortem examination (281 patients) or by strong clinical confirmation with at least a six-month follow-up (615 patients). In this group of 896 patients, 775 had a primary lung neoplasm and 121 had metastatic lung or pleural tumors. One aspiration procedure provided malignant cells in 87% of patients (783 out of 896) with intrathoracic cancer; the yield of malignant cells rose to 96% in patients who underwent two procedures (858 out of 896 patients). Of the 858 patients for whom a positive diagnosis was obtained, 75 required a second biopsy for diagnosis. For this reason, one negative procedure is considered an incomplete diagnostic test in the cancer suspect. A positive diagnosis was achieved in all
401 Sage1 et al: Percutaneous Transthoracic Aspiration Needle Biopsy
31 patients with a superior sulcus (Pancoast’s) tumor. A false positive diagnosis of carcinoma was made in 2 patients subsequently found to have active focal tuberculosis. The squamous metaplasia surrounding these lesions was misinterpreted on cytological preparations as caused by neoplasia. While the sensitivity (true positive rate) in diagnosing malignant neoplasm by aspiration needle biopsy was extremely high (99% or 858 out of 860 patients) in our series, the specificity (true negative rate) was only 87% (255 out of 293 patients). Thus a finding of “no malignant cells” should not be construed as conclusive proof of the absence of malignancy. The diagnostic accuracy of aspiration needle biopsy in malignant neoplasm was 96.5% or 1,113 out of 1,153 patients. Granulomatous infection was diagnosed in 19 circumscribed lesions by aspiration needle biopsy technique. The initial smear from the aspirate showed histoplasmosis organisms in 2 lesions and acid-fast bacilli (Mycobacterium tuberculosis) in 2. In the remaining 15 lesions, M. tuberculosis (lo), atypical mycobacterium (2), cryptococci (2), and blastomyces (1)were recovered from culture. Three of these 15 lesions disclosed fibrous tissue or Langhans’ giant cells or both on histological examination of the aspirated material. These findings emphasize that in the patient with an indeterminate nodule, it may be worthwhile to wait several weeks for culture results before a management decision is made. Two subpleural lipomas and 2 pericardial cysts were correctly diagnosed by aspiration needle biopsy by findings of abundant fat cells or cytology negative clear fluid, respectively. However, the recent introduction of computed tomography [6] could obviate the use of this invasive technique for these types of lesions. In 31 immunosuppressed patients in whom a focal pneumonic infiltrate was aspirated, cultures from 24 showed an infectious agent. In 11 of these patients, a stained smear of the aspirate disclosed the causative bacterial or fungal agent. A variety of unusual organisms in addition to the usual bacteria were retrieved. This accuracy rate of 77% may be spuriously low since no organism was found in cultures from several
patients receiving concomitant antibiotic therapy in whom the pneumonic infiltrate resolved.
Complications No deaths attributable to the procedure occurred in our series. One patient sustained a nonfatal myocardial infarction immediately following the procedure. Pneumothorax was by far the most common complication, developing in 292 (24%) of our patients. The risk of pneumothorax rose substantially when emphysema or lesions deep within the lung or both conditions were present. Chest tube drainage was required in 167patients (14%), usually for a period of 24 to 48 hours. However, 5 patients with severe bullous emphysema needed sustained drainage for 7 to 10 days before the air leak closed. The clinician must carefully weigh this possibility of prolonged patient discomfort against the advantages of a specific tissue diagnosis when evaluating such a patient. Conversely, chest tube drainage was required in less than 5% of patients who were less than 40 years old. Transient minor hemoptysis occurred in 73 patients (6%). With the aspirating needle, substantial pulmonary hemorrhage was never a problem requiring special management. Chest radiographs made after biopsy revealed minor bleeding around the aspirated lesion in 48 patients (4%); these infiltrates always resorbed spontaneously within a week. A small asymptomatic pleural effusion (presumably a hemothorax) developed in 6 patients (0.5%). Incidental puncture of the pulmonary artery or thoracic aorta (including two tumorlike aneurysms) occurred on several occasions, without producing symptoms or requiring therapy. In general, such incidents can be avoided by careful planning of the puncture approach. No instances of massive intrapulmonary hemorrhage or of spread of infection to the pleural space resulting in an empyema were encountered. Nor were local or systemic flares recognized following aspiration of an inflammatory process. To our knowledge, aspiration needle biopsy did not result in needle track implantation of tumor cells in any patient. Air embolism, another rare but life-threatening complication, also did not occur. With proper
402 The Annals of Thoracic Surgery Vol 26 No 5 November 1978
precautions, this complication should be avoidable. It is mandatory that the needle hub not be left open to the atmosphere for any length of time following withdrawal of the stylet. With our technique, this hole is temporarily covered by the thumb before the syringe is attached.
Comment Percutaneous transthoracic fine-needle aspiration biopsy is a highly accurate method of diagnosing fluoroscopically visible pulmonary neoplasms and infectious infiltrates beyond the reach of the fiberoptic bronchoscope. The technique deserves wider acceptance and use because it is easily performed and the traditional concerns have not been substantiated by critical analysis. Most previously reported cases of needle track implantation occurred either when large cutting needles were used or in patients with far-advanced neoplasms in whom tumor seeding had no effect on their management [19]. Recent experimental studies demonstrate the very low probability of tumor spread following aspiration needle biopsy [3]. Corroborating clinical evidence exists in the miniscule incidence of tumor implantation reported from the largest patient series [14]. We believe there is little reason to fear transformation of a curable lesion into an incurable one by aspiration needle biopsy. The clinical impact of aspiration needle biopsy can be shown by the fact that only 19% of patients undergoing this procedure in our series eventually underwent thoracotomy, with the majority of operations performed for treatment rather than diagnosis. Most of the patients had multiple diagnostic procedures, including, at least, analysis of sputum specimens and bronchoscopy, before needle aspiration. Presumably, many more would have undergone diagnostic thoracotomy if needle aspiration biopsy was not available. Our results in diagnosing lung cancer, except for the differentiation of cell type, are as good as the best series using a cutting needle [5]. Similar success rates have been reported by others [9, 11-13, 201. The distinction between an aspirating needle and a cutting biopsy needle
cannot be overemphasized. While the cutting needle provides a larger core of tissue for histological analysis, it is far more hazardous and far more likely to cause marked intrapulmonary hemorrhage, which at times may be fatal [4,81. Our cytopathologist can usually distinguish oat cell carcinoma, malignant melanoma, and a few other rare malignant lesions, but for most patients the pathological report reads simply ”malignant cells present.” In the overwhelming number of patients, the lack of a specific cell type is usually not of therapeutic importance. Clearly, the results achieved by aspiration needle biopsy are dependent upon the expertise of the cytopathologist. But the lack of accurate cytological services in a hospital is not an insurmountable problem since techniques are available for cell preservation before transportation to consultative laboratories. Aspiration needle biopsy is used frequently in our medical center. It is a valuable technique for ascertaining the cause of a persistent localized pulmonary mass or infiltrate undiagnosed by conventional modalities, such as sputum examinations and culture, bronchoscopy, and serological studies. It is particularly valuable with lesions in the middle third or periphery of the lung that cannot be reached with the fiberoptic bronchoscope [l, 71, although biopsies of undiagnosed central lesions (including hilar lymph nodes) can be done with this technique. A point deserving emphasis is that aspiration needle biopsy has no role in providing a tissue diagnosis of diffuse lung disease; histological specimens are much better obtained by transbronchial lung biopsy through the fiberoptic bronchoscope or by thoracotomy. There are several specific indications for aspiration needle biopsy. 1. Pulmonary mass or masses in a patient unsuitable for curative thoracotomy because of metastatic disease or a severe associated medical disorder, in whom definitive tissue diagnosis is required before the institution of radiotherapy or chemotherapy. At times, the clinician may merely wish to confirm a strong suspicion of lung neoplasm in order to offer the patient or his family a more definitive diag-
403
Sagel et al: Percutaneous Transthoracic Aspiration Needle Biopsy
nosis and prognosis, without any therapeutic objectives. A rare instance in which needle aspiration biopsy may be considered a more primary investigative tool, preceding or supplanting bronchoscopy, is in the patient with suspected superior sulcus tumor. In such patients the diagnostic yield has been exceedingly high and the risk of pneumothorax low [181. 2. Suspected localized pneumonic infiltrate in an immunocompromised patient, or a worsening pneumonia in a patient despite antibiotic therapy. Obtaining a specific microorganism is particularly important in the immune-deficient individual because of the large variety of opportunistic infectious agents that may be responsible for the infiltrate. Needle aspiration of the localized pneumonic infiltrate usually can provide direct (without contamination by the upper respiratory tract flora) identification of the causative agent. 3. Solitary undiagnosed pulmonary lesion. In a patient who is a marginal surgical candidate, a positive diagnosis of carcinoma may convince both the patient and the referring physician that thoracotomy is warranted despite the risks entailed. In the patient with known systemic malignancy (e.g., Hodgkin’s disease), differentiation of neoplastic pulmonary infiltration from a pneumonic process is usually possible. An area of controversy is the patient with a solitary undiagnosed pulmonary nodule and no contraindications to thoracotomy. We believe that aspiration needle biopsy can play a valuable role in many of these patients, but do not advocate this technique for every such lesion. In certain situations when the clinical history or roentgenographic findings strongly suggest malignancy (e.g., a 50-year-old male smoker with an irregular expanding lesion), it is not unreasonable to proceed directly to thoracotomy. However, there is a definite advantage in establishing a precise diagnosis in many patients before resorting to thoracotomy. Only about 40% of peripheral pulmonary nodules that are operated on prove to be malignant, and a definable postoperative morbidity and mortality can be expected [161. A positive preoperative diagnosis of malig-
nancy may expedite and simplify the operative approach. Also, ascertaining the cell type of suspected malignant lesions when possible is worthwhile since resection of a small cell carcinoma will almost always prove futile [151. If a diagnosis of granuloma is achieved (by histology, smear, or culture), an operation can be avoided. Positive identification of a benign lesion, however, is usually difficult with the aspiration technique. In the absence of malignant tissue, small tissue fragments demonstrating fibrosis or chronic pneumonitis suggest a benign process. Since a malignant lesion certainly can be missed by aspiration needle biopsy, the management of the patient in whom nondiagnostic material is retrieved must be based upon clinical judgment. The decision for thoracotomy or careful clinical follow-up must be made in conjunction with all available information about the patient.
References 1. Borgeskov S, Francis B: A comparison between
2.
3.
4. 5.
6. 7.
8. 9. 10.
11.
fine needle biopsy and fiberoptic bronchoscopy in patients with lung lesions. Thorax 29:352,1974 Dahlgren S, Nordenstrom B: Transthoracic Needle Biopsy. Chicago, Year Book, 1966 Engzell V, Esposti PL, Rubio C, et al: Investigation on tumor spread in connection with aspiration biopsy. Acta Radio1 [Ther] (Stockh) 10:385, 1971 Forrest JV, Sagel SS: Cutting needle biopsies. Chest 69:245, 1976 Herman PG, Hessel SJ: The diagnostic accuracy and complications of closed lung biopsies. Radiology 125:11, 1977 Jost RG, Sagel SS, Stanley RJ, et al: Computed tomography of the thorax. Radiology 126:125, 1978 Landman S, Burgener FA, Lim GAK: Comparison of bronchial brushing and percutaneous needle aspiration biopsy in the diagnosis of malignant lung lesions. Radiology 11527.5, 1975 Norenberg R, Claxton CP, Takaro T: Percutaneous needle biopsy of the lung: report of two fatal complications. Chest 66:216, 1974 Pavy RD, Antic R, Begley M: Percutaneous aspiration biopsy of discrete lung lesions. Cancer 34:109, 1974 Sagel SS, Forrest JV: Fluoroscopically assisted lung biopsy techniques, in Special Procedures in Chest Radiology. Edited by S.S Sagel. Philadelphia, Saunders, 1976, p 22 Sanders DE, Thompson DW, Pudden BJE: Per-
404 The Annals of Thoracic Surgery Vol 26 No 5 November 1978
cutaneous aspiration lung biopsy. Can Med Assoc J 104:139, 1971 12. Sargent EN, Turner AF, Gordonson J, et al: Percutaneous pulmonary needle biopsy. Am J Roentgenol 122:758, 1974 13. Sinner WN: Transthoracic needle biopsy of small peripheral malignant lung lesions. Invest Radiol 8:305, 1973 14. Sinner WN: Complications of percutaneous transthoracic needle aspiration biopsy. Acta Radiol [Diagn] (Stockh) 17:813, 1976 15. Sinner WN, Sandstedt B: Small-cell carcinoma of the lung. Cytological, roentgenologic, and clinical findings in a consecutive series diagnosed by fine-needle aspiration biopsy. Radiology 121269, 1976 16. Trunk G, Gracey DR, Byrd RB: The management and evaluation of the solitary pulmonary nodule. Chest 66236, 1974 17. Turner FT, Sargent EN: Percutaneous pulmonary needle biopsy: an improved needle for a simple direct method of diagnosis. Am J Roentgenol 100:846, 1968 18. Walls WJ, Thornbury JR, Naylor B: Pulmonary needle aspiration biopsy in the diagnosis of Pancoast tumors. Radiology 111:99, 1974 19. Wolinsky H, Lischner MW: Needle track implantation of tumor after percutaneous lung biopsy. Ann Intern Med 21:359, 1969 20. Zelch JV, Lalli AF, McCormack LJ, et al: Aspiration biopsy in diagnosis of pulmonary nodule. Chest 63:149, 1973
Discussion (Evanston, IL): At the Evanston Hospital (Northwestern University Medical School) I have a personal series of 108 patients who had a transthoracic needle biopsy and can agree wholeheartedly with Dr. Sagel’s group on the indications for the procedure and its application to patient care. It is of interest to me that our results are almost identical-as are our rates of pneumothorax and chest tube drainage. Like the Washington University group, most of our interest has been devoted to primary and metastatic lung cancer. Tabulating our results on a case basis rather than a patient basis, we have an 84% positive rate, which compares with Dr. Sagel’s firsttime rate of 87%. Our single false positive was also in a patient with tuberculosis, and the cytological changes of pulmonary inflammation are notorious for confusion with adenocarcinoma. Our rate of pneumothorax is 25%, but only half of these patients need pleural intubation. We do many transthoracic needle biopsies on an outpatient basis, but we inform patients that they should come psychologically prepared to spend the night if necessary. We also warn them they may require chest tube drainage. DR. WILLARD A. FRY
Hemoptysis after transthoracic needle biopsy has been infrequent and always self-limited. However, it is important to warn patients of this possible result in advance, so that they do not become scared if they cough up a little blood. We have had no deaths. The Loma Linda group suggested injecting 10 ml of autologous blood into the tract because they found a decreased incidence of pneumothorax in those patients who had ”soiting” with blood on the films made after transthoracic needle biopsy (McCartney R, Tait D, Stilson M, et al: A technique for the prevention of pneumothorax in pulmonary aspiration biopsy. Am J Roentgenol Radium Ther Nucl Med 120:872,1974).We have not tried this but it is an interesting idea. Tumor seeding of the needle tract does not occur to any significant degree with the fine needle technique. This has been well documented in the literature, particularly by Nordenstrom and Bjork in a review of more than 4,000 cases (Nordenstrom B, Bjork VO: Letter to the editor. J Thorac Cardiovasc Surg 65:671, 1973). Our technique varies a little from that of Dr. Sagel’s group. We use a 22-gauge needle and pass it through an 18-gauge needle, which negotiates the skin and chest wall fasciae but does not reach the pleura. We limit the puncture to a single maneuver if we have good material. Most of the time there is nothing in the syringe, and the specimen is blown onto glass slides. We consider the pistol syringe very helpful: it produces a surprising vacuum and frees one hand (Camco Syringe Pistol, Precision Dynamics Corp, 3031 Thornton Ave, Burbank, CA 91504. Aspir-Gun, The Everest Co, 5 Sherman St, Linden, NJ 07036). Like Dr. Sagel’s group, we do not perform an aspiration needle biopsy on every potentially operable patient. A positive transthoracic needle biopsy, however, certainly expedites the procedure, for we don’t have to spend time doing a wedge biopsy or frozen sections. Instead, we can proceed immediately with the proper resection. The importance of a good cytopathologist cannot be overemphasized because a cytological diagnosis should be as good as a histological one, and most of the time a specific cell type should be identified. This is an important procedure that deserves more widespread use. DR. RICHARD M . PETERS (San Diego, CA): Before Dr. Jack Forrest came to San Diego from St. Louis, I was very skeptical of aspiration needle biopsy, but I must state that Dr. Forrest has convinced me that this procedure, as presented by Dr. Sagel, is a very important addition to the diagnostic armamentarium. It is far better for the patient when he can be told the diagnosis before operation. Also when we know we are dealing with carcinoma, not with possibly a granuloma, we are better able to decide whether to
405
Sage1 et al: Percutaneous Transthoracic Aspiration Needle Biopsy
proceed with operation in patients with very marginal function. Equally important, aspiration needle biopsy has saved a number of patients from an operative procedure. However, I would like to stress that it is extremely important not to accept the diagnosis of a negative biopsy. There must also be a histological diagnosis. It may be a granuloma or it may be some other infection, but, like a negative sputum, a negative needle biopsy has no meaning. Aspiration needle biopsy provides an easy and safe way for us to be much more specific in our therapy of patients.
how you achieve that. Invariably, we must wait 24 hours for an answer, while you implied that you take a biopsy specimen in the morning, receive an answer at lunchtime, and repeat a biopsy procedure in the afternoon. I would like a comment on that aspect of your procedure.
DR. THOMAS D. BARTLEY (Gainesville, FL): We, too, use aspiration needle biopsy of pulmonary lesions very aggressively and are very happy with the method. We practically never do a thoracotomy now without a previous positive histological diagnosis. I am interested that you are able to obtain sameday diagnosis from your pathologists, and I wonder
DR. SAGEL: The aspirated material for cytopathological study is placed in a tube containing a balanced electrolyte solution (Polysal) and conveyed to the pathology laboratory. Stained slides of the cytological preparation are available for interpretation within an hour. However, any available cell block would not be ready for at least 12 hours.
c . GRILLO (Boston, MA): A minor technical note. Dr. Reginald Greene, our pulmonary radiologist, reduced the incidence of pneumothorax markedly by using a two-needle technique. An outer needle is placed first in the target. Multiple aspirations are done by inserting a second needle through the outer one. DR. HERMES
Percutaneous Transthoracic Aspiration Needle Biopsy Stuart S. Sagel, M.D., Thomas B. Ferguson, M.D., John V. Forrest, M.D., Charles L. Roper, M.D., Clarence S. Weldon, M.D., and Richard E. Clark, M.D: ABSTRACT An experience based on 1,211 patients has shown aspiration needle biopsy to be a valuable technique for diagnosing bronchogenic carcinoma and other localized intrathoracic lesions that are beyond the reach of the fiberoptic bronchoscope.In 896 patients with malignant intrathoracic neoplasm, the aspirate demonstrated malignant cells in 96%. A false cytological diagnosis of carcinoma occurred in 2 patients, for a true positive rate of 99%. However, the true negative rate was only 87%. In 77% of 31 immunosuppressed patients, the causative agent of a focal infectious process was diagnosed. Pneumothorax was the only notable complication, occurring in 24% of patients, with 14% requiring chest tube drainage. The procedure is relatively simple and rapid, generally causes little patient discomfort, and can be performed in virtually any hospital.
While the chest radiograph is a sensitive method for detecting pulmonary pathology, it usually lacks the specificity required for etiological diagnosis and treatment planning. The determination of the cause of a pulmonary nodule, mass, or focal infiltrate remains a common clinical problem generally requiring cytological, histological, or microbiological studies. Percutaneous lung puncture has been used as a diagnostic technique since the late nineteenth century, but the lack of adequate visual control and proper equipment can lead to major complications. During the last decade, interest in the contribution of percutaneous aspiration needle biopsy has been accelerated by the high degree of diagnostic accuracy made possible by television-monitored fluoroscopy, improved needles, and advanced cytoFrom the Mallinckrodt Institute of Radiology, and the Division of Cardiothoracic Surgery, Washington University School of Medicine, St. Louis, MO. Presented at the Fourteenth Annual Meeting of The Society of Thoracic Surgeons, Jan 23-25, 1978, Orlando, FL. Address reprint requests to Dr. Sagel, 510 S Kingshighway Blvd, St. Louis, MO 63110.
399 0003497517810026-0503$01.25 @ 1978 by Stuart S. Sagel
pathological techniques [ 2 ] . The failure of this procedure to spread widely, especially to nonuniversity hospitals, has been discouraging to its proponents. Our purpose is to emphasize the simplicity, rapidity, safety, and high diagnostic accuracy of the technique.
Materials and Method During the past 5% years, 1,211 patients, ranging from 15 to 91 years old, have undergone percutaneous transthoracic aspiration needle, biopsy at the Mallinckrodt Institute of Radiology. The overwhelming majority of patients were referred for consultation from the Division of Cardiothoracic Surgery and the Pulmonary Medicine Service of Barnes Hospital when the cause of a persistent localized pulmonary mass or infiltrate remained undiagnosed by conventional modalities, such as sputum examination and culture, bronchoscopy, and serological studies. The complete technique of pulmonary aspiration needle biopsy has been described in detail previously [lo] and will be only summarized here. That the procedure is easily learned and accomplished, rarely takes longer than fifteen minutes to perform, and requires no complex equipment or devices deserves emphasis. Testing for a bleeding diathesis is done by a coagulation laboratory survey in the cachectic cancer suspect or the immunosuppressed patient before proceeding with the biopsy. Premedication is usually unnecessary. If the patient is particularly apprehensive despite reassurance given while obtaining informed consent, Valium (diazepam) is administered before aspiration. In patients with severe pain before biopsy (e.g., those with a tumor of the superior sulcus), use of narcotic analgesia facilitates performance of the procedure. Following localization of the lesion by chest radiography and fluoroscopy, the patient is placed on a fluoroscopic table in the position that permits the most direct needle access. In
400 The Annals of Thoracic Surgery Vol 26
No 5 November 1978
general, this is either the supine or prone position. With a lesion near the lateral chest wall, the patient may be placed in a lateral decubitus position; and with a lesion located just above the hemidiaphragm, a rare finding, an upright attitude is used. Under fluoroscopic control, a point on the skin, usually one directly overlying the lesion, is marked. The patient’s skin is cleansed, the puncture site is infiltrated with local anesthesia, and a small skin and subcutaneous tissue stab incision is made with a scalpel blade before the needle is introduced. With intermittent fluoroscopy to aid straight passage, the tip of the aspirating needle is advanced to the appropriate depth. This is gauged either by estimation from previous chest radiographs or tomograms or both, or by inserting the tip until a change in consistency of the lung is felt. The relationship between the needle tip and the lesion is monitored by having the patient breathe shallowly. Sometimes it is necessary to turn the patient slightly to better ascertain that the needle tip abuts the lesion. A television-monitored single-plane image intensification fluoroscopy (preferably with an over-the-table tube) is required. Such readily available equipment almost always suffices for needle localization. We generally use an 18-gauge Turnermodified aspirating needle [17].* The sharp outer cannula of this needle permits larger fragments of tissue to be obtained than do similar gauge spinal needles. Harvest of these tissue fragments increases the incidence of specific histological diagnosis over cytological techniques alone. With the needle tip positioned adjacent to the lesion, the internal stylet is removed, and a 10-ml syringe is quickly attached to the needle hub. With the application of continuous suction, the needle tip is moved back and forth over a 0.5- to 1.0-cm distance several times, using a jabbing and rotating motion through the lesion. Then the needle is withdrawn. Suction is released and the aspirated material is flushed into a sterile balanced electrolyte solution (Polysal). If a small core of tissue is identified, it is transferred to 10% formalin solution for subsequent histological *Available from Cook, Inc, Bloomington, IN 47401.
study. The number of lung punctures is variable, usually ranging from 1 to 5 per patient. The procedure is repeated as many times as necessary until small tissue fragments can be seen in the solution. This material is sent for appropriate pathological (cytology and cell block) or microbiological studies or both. After the biopsy procedure, a frontal upright expiration chest radiograph is made to evaluate for a complicating pneumothorax. If pulmonary neoplasm is suspected and if the samples from the initial procedure are negative, a second biopsy procedure is performed, either the same day or the following morning. An attempt is made to sample from different parts of the lesion. If no malignant cells are detected on only one biopsy attempt in patients in whom the suspicion of carcinoma is high, the study should be considered technically incomplete. If a pneumothorax occurs after the first biopsy procedure, a chest tube is inserted before the procedure is repeated. The presence of the chest tube permits aggressive sampling on the second biopsy since the major potential complication of pneumothorax has been removed.
Results Diagnostic Accuracy Aspiration needle biopsy of a localized intrathoracic mass or infiltrate was performed in 1,153 patients in whom cancer was a clinical consideration. Of these patients, 896 had a malignant intrathoracic neoplasm as evidenced by either surgical proof or postmortem examination (281 patients) or by strong clinical confirmation with at least a six-month follow-up (615 patients). In this group of 896 patients, 775 had a primary lung neoplasm and 121 had metastatic lung or pleural tumors. One aspiration procedure provided malignant cells in 87% of patients (783 out of 896) with intrathoracic cancer; the yield of malignant cells rose to 96% in patients who underwent two procedures (858 out of 896 patients). Of the 858 patients for whom a positive diagnosis was obtained, 75 required a second biopsy for diagnosis. For this reason, one negative procedure is considered an incomplete diagnostic test in the cancer suspect. A positive diagnosis was achieved in all
401 Sage1 et al: Percutaneous Transthoracic Aspiration Needle Biopsy
31 patients with a superior sulcus (Pancoast’s) tumor. A false positive diagnosis of carcinoma was made in 2 patients subsequently found to have active focal tuberculosis. The squamous metaplasia surrounding these lesions was misinterpreted on cytological preparations as caused by neoplasia. While the sensitivity (true positive rate) in diagnosing malignant neoplasm by aspiration needle biopsy was extremely high (99% or 858 out of 860 patients) in our series, the specificity (true negative rate) was only 87% (255 out of 293 patients). Thus a finding of “no malignant cells” should not be construed as conclusive proof of the absence of malignancy. The diagnostic accuracy of aspiration needle biopsy in malignant neoplasm was 96.5% or 1,113 out of 1,153 patients. Granulomatous infection was diagnosed in 19 circumscribed lesions by aspiration needle biopsy technique. The initial smear from the aspirate showed histoplasmosis organisms in 2 lesions and acid-fast bacilli (Mycobacterium tuberculosis) in 2. In the remaining 15 lesions, M. tuberculosis (lo), atypical mycobacterium (2), cryptococci (2), and blastomyces (1)were recovered from culture. Three of these 15 lesions disclosed fibrous tissue or Langhans’ giant cells or both on histological examination of the aspirated material. These findings emphasize that in the patient with an indeterminate nodule, it may be worthwhile to wait several weeks for culture results before a management decision is made. Two subpleural lipomas and 2 pericardial cysts were correctly diagnosed by aspiration needle biopsy by findings of abundant fat cells or cytology negative clear fluid, respectively. However, the recent introduction of computed tomography [6] could obviate the use of this invasive technique for these types of lesions. In 31 immunosuppressed patients in whom a focal pneumonic infiltrate was aspirated, cultures from 24 showed an infectious agent. In 11 of these patients, a stained smear of the aspirate disclosed the causative bacterial or fungal agent. A variety of unusual organisms in addition to the usual bacteria were retrieved. This accuracy rate of 77% may be spuriously low since no organism was found in cultures from several
patients receiving concomitant antibiotic therapy in whom the pneumonic infiltrate resolved.
Complications No deaths attributable to the procedure occurred in our series. One patient sustained a nonfatal myocardial infarction immediately following the procedure. Pneumothorax was by far the most common complication, developing in 292 (24%) of our patients. The risk of pneumothorax rose substantially when emphysema or lesions deep within the lung or both conditions were present. Chest tube drainage was required in 167patients (14%), usually for a period of 24 to 48 hours. However, 5 patients with severe bullous emphysema needed sustained drainage for 7 to 10 days before the air leak closed. The clinician must carefully weigh this possibility of prolonged patient discomfort against the advantages of a specific tissue diagnosis when evaluating such a patient. Conversely, chest tube drainage was required in less than 5% of patients who were less than 40 years old. Transient minor hemoptysis occurred in 73 patients (6%). With the aspirating needle, substantial pulmonary hemorrhage was never a problem requiring special management. Chest radiographs made after biopsy revealed minor bleeding around the aspirated lesion in 48 patients (4%); these infiltrates always resorbed spontaneously within a week. A small asymptomatic pleural effusion (presumably a hemothorax) developed in 6 patients (0.5%). Incidental puncture of the pulmonary artery or thoracic aorta (including two tumorlike aneurysms) occurred on several occasions, without producing symptoms or requiring therapy. In general, such incidents can be avoided by careful planning of the puncture approach. No instances of massive intrapulmonary hemorrhage or of spread of infection to the pleural space resulting in an empyema were encountered. Nor were local or systemic flares recognized following aspiration of an inflammatory process. To our knowledge, aspiration needle biopsy did not result in needle track implantation of tumor cells in any patient. Air embolism, another rare but life-threatening complication, also did not occur. With proper
402 The Annals of Thoracic Surgery Vol 26 No 5 November 1978
precautions, this complication should be avoidable. It is mandatory that the needle hub not be left open to the atmosphere for any length of time following withdrawal of the stylet. With our technique, this hole is temporarily covered by the thumb before the syringe is attached.
Comment Percutaneous transthoracic fine-needle aspiration biopsy is a highly accurate method of diagnosing fluoroscopically visible pulmonary neoplasms and infectious infiltrates beyond the reach of the fiberoptic bronchoscope. The technique deserves wider acceptance and use because it is easily performed and the traditional concerns have not been substantiated by critical analysis. Most previously reported cases of needle track implantation occurred either when large cutting needles were used or in patients with far-advanced neoplasms in whom tumor seeding had no effect on their management [19]. Recent experimental studies demonstrate the very low probability of tumor spread following aspiration needle biopsy [3]. Corroborating clinical evidence exists in the miniscule incidence of tumor implantation reported from the largest patient series [14]. We believe there is little reason to fear transformation of a curable lesion into an incurable one by aspiration needle biopsy. The clinical impact of aspiration needle biopsy can be shown by the fact that only 19% of patients undergoing this procedure in our series eventually underwent thoracotomy, with the majority of operations performed for treatment rather than diagnosis. Most of the patients had multiple diagnostic procedures, including, at least, analysis of sputum specimens and bronchoscopy, before needle aspiration. Presumably, many more would have undergone diagnostic thoracotomy if needle aspiration biopsy was not available. Our results in diagnosing lung cancer, except for the differentiation of cell type, are as good as the best series using a cutting needle [5]. Similar success rates have been reported by others [9, 11-13, 201. The distinction between an aspirating needle and a cutting biopsy needle
cannot be overemphasized. While the cutting needle provides a larger core of tissue for histological analysis, it is far more hazardous and far more likely to cause marked intrapulmonary hemorrhage, which at times may be fatal [4,81. Our cytopathologist can usually distinguish oat cell carcinoma, malignant melanoma, and a few other rare malignant lesions, but for most patients the pathological report reads simply ”malignant cells present.” In the overwhelming number of patients, the lack of a specific cell type is usually not of therapeutic importance. Clearly, the results achieved by aspiration needle biopsy are dependent upon the expertise of the cytopathologist. But the lack of accurate cytological services in a hospital is not an insurmountable problem since techniques are available for cell preservation before transportation to consultative laboratories. Aspiration needle biopsy is used frequently in our medical center. It is a valuable technique for ascertaining the cause of a persistent localized pulmonary mass or infiltrate undiagnosed by conventional modalities, such as sputum examinations and culture, bronchoscopy, and serological studies. It is particularly valuable with lesions in the middle third or periphery of the lung that cannot be reached with the fiberoptic bronchoscope [l, 71, although biopsies of undiagnosed central lesions (including hilar lymph nodes) can be done with this technique. A point deserving emphasis is that aspiration needle biopsy has no role in providing a tissue diagnosis of diffuse lung disease; histological specimens are much better obtained by transbronchial lung biopsy through the fiberoptic bronchoscope or by thoracotomy. There are several specific indications for aspiration needle biopsy. 1. Pulmonary mass or masses in a patient unsuitable for curative thoracotomy because of metastatic disease or a severe associated medical disorder, in whom definitive tissue diagnosis is required before the institution of radiotherapy or chemotherapy. At times, the clinician may merely wish to confirm a strong suspicion of lung neoplasm in order to offer the patient or his family a more definitive diag-
403
Sagel et al: Percutaneous Transthoracic Aspiration Needle Biopsy
nosis and prognosis, without any therapeutic objectives. A rare instance in which needle aspiration biopsy may be considered a more primary investigative tool, preceding or supplanting bronchoscopy, is in the patient with suspected superior sulcus tumor. In such patients the diagnostic yield has been exceedingly high and the risk of pneumothorax low [181. 2. Suspected localized pneumonic infiltrate in an immunocompromised patient, or a worsening pneumonia in a patient despite antibiotic therapy. Obtaining a specific microorganism is particularly important in the immune-deficient individual because of the large variety of opportunistic infectious agents that may be responsible for the infiltrate. Needle aspiration of the localized pneumonic infiltrate usually can provide direct (without contamination by the upper respiratory tract flora) identification of the causative agent. 3. Solitary undiagnosed pulmonary lesion. In a patient who is a marginal surgical candidate, a positive diagnosis of carcinoma may convince both the patient and the referring physician that thoracotomy is warranted despite the risks entailed. In the patient with known systemic malignancy (e.g., Hodgkin’s disease), differentiation of neoplastic pulmonary infiltration from a pneumonic process is usually possible. An area of controversy is the patient with a solitary undiagnosed pulmonary nodule and no contraindications to thoracotomy. We believe that aspiration needle biopsy can play a valuable role in many of these patients, but do not advocate this technique for every such lesion. In certain situations when the clinical history or roentgenographic findings strongly suggest malignancy (e.g., a 50-year-old male smoker with an irregular expanding lesion), it is not unreasonable to proceed directly to thoracotomy. However, there is a definite advantage in establishing a precise diagnosis in many patients before resorting to thoracotomy. Only about 40% of peripheral pulmonary nodules that are operated on prove to be malignant, and a definable postoperative morbidity and mortality can be expected [161. A positive preoperative diagnosis of malig-
nancy may expedite and simplify the operative approach. Also, ascertaining the cell type of suspected malignant lesions when possible is worthwhile since resection of a small cell carcinoma will almost always prove futile [151. If a diagnosis of granuloma is achieved (by histology, smear, or culture), an operation can be avoided. Positive identification of a benign lesion, however, is usually difficult with the aspiration technique. In the absence of malignant tissue, small tissue fragments demonstrating fibrosis or chronic pneumonitis suggest a benign process. Since a malignant lesion certainly can be missed by aspiration needle biopsy, the management of the patient in whom nondiagnostic material is retrieved must be based upon clinical judgment. The decision for thoracotomy or careful clinical follow-up must be made in conjunction with all available information about the patient.
References 1. Borgeskov S, Francis B: A comparison between
2.
3.
4. 5.
6. 7.
8. 9. 10.
11.
fine needle biopsy and fiberoptic bronchoscopy in patients with lung lesions. Thorax 29:352,1974 Dahlgren S, Nordenstrom B: Transthoracic Needle Biopsy. Chicago, Year Book, 1966 Engzell V, Esposti PL, Rubio C, et al: Investigation on tumor spread in connection with aspiration biopsy. Acta Radio1 [Ther] (Stockh) 10:385, 1971 Forrest JV, Sagel SS: Cutting needle biopsies. Chest 69:245, 1976 Herman PG, Hessel SJ: The diagnostic accuracy and complications of closed lung biopsies. Radiology 125:11, 1977 Jost RG, Sagel SS, Stanley RJ, et al: Computed tomography of the thorax. Radiology 126:125, 1978 Landman S, Burgener FA, Lim GAK: Comparison of bronchial brushing and percutaneous needle aspiration biopsy in the diagnosis of malignant lung lesions. Radiology 11527.5, 1975 Norenberg R, Claxton CP, Takaro T: Percutaneous needle biopsy of the lung: report of two fatal complications. Chest 66:216, 1974 Pavy RD, Antic R, Begley M: Percutaneous aspiration biopsy of discrete lung lesions. Cancer 34:109, 1974 Sagel SS, Forrest JV: Fluoroscopically assisted lung biopsy techniques, in Special Procedures in Chest Radiology. Edited by S.S Sagel. Philadelphia, Saunders, 1976, p 22 Sanders DE, Thompson DW, Pudden BJE: Per-
404 The Annals of Thoracic Surgery Vol 26 No 5 November 1978
cutaneous aspiration lung biopsy. Can Med Assoc J 104:139, 1971 12. Sargent EN, Turner AF, Gordonson J, et al: Percutaneous pulmonary needle biopsy. Am J Roentgenol 122:758, 1974 13. Sinner WN: Transthoracic needle biopsy of small peripheral malignant lung lesions. Invest Radiol 8:305, 1973 14. Sinner WN: Complications of percutaneous transthoracic needle aspiration biopsy. Acta Radiol [Diagn] (Stockh) 17:813, 1976 15. Sinner WN, Sandstedt B: Small-cell carcinoma of the lung. Cytological, roentgenologic, and clinical findings in a consecutive series diagnosed by fine-needle aspiration biopsy. Radiology 121269, 1976 16. Trunk G, Gracey DR, Byrd RB: The management and evaluation of the solitary pulmonary nodule. Chest 66236, 1974 17. Turner FT, Sargent EN: Percutaneous pulmonary needle biopsy: an improved needle for a simple direct method of diagnosis. Am J Roentgenol 100:846, 1968 18. Walls WJ, Thornbury JR, Naylor B: Pulmonary needle aspiration biopsy in the diagnosis of Pancoast tumors. Radiology 111:99, 1974 19. Wolinsky H, Lischner MW: Needle track implantation of tumor after percutaneous lung biopsy. Ann Intern Med 21:359, 1969 20. Zelch JV, Lalli AF, McCormack LJ, et al: Aspiration biopsy in diagnosis of pulmonary nodule. Chest 63:149, 1973
Discussion (Evanston, IL): At the Evanston Hospital (Northwestern University Medical School) I have a personal series of 108 patients who had a transthoracic needle biopsy and can agree wholeheartedly with Dr. Sagel’s group on the indications for the procedure and its application to patient care. It is of interest to me that our results are almost identical-as are our rates of pneumothorax and chest tube drainage. Like the Washington University group, most of our interest has been devoted to primary and metastatic lung cancer. Tabulating our results on a case basis rather than a patient basis, we have an 84% positive rate, which compares with Dr. Sagel’s firsttime rate of 87%. Our single false positive was also in a patient with tuberculosis, and the cytological changes of pulmonary inflammation are notorious for confusion with adenocarcinoma. Our rate of pneumothorax is 25%, but only half of these patients need pleural intubation. We do many transthoracic needle biopsies on an outpatient basis, but we inform patients that they should come psychologically prepared to spend the night if necessary. We also warn them they may require chest tube drainage. DR. WILLARD A. FRY
Hemoptysis after transthoracic needle biopsy has been infrequent and always self-limited. However, it is important to warn patients of this possible result in advance, so that they do not become scared if they cough up a little blood. We have had no deaths. The Loma Linda group suggested injecting 10 ml of autologous blood into the tract because they found a decreased incidence of pneumothorax in those patients who had ”soiting” with blood on the films made after transthoracic needle biopsy (McCartney R, Tait D, Stilson M, et al: A technique for the prevention of pneumothorax in pulmonary aspiration biopsy. Am J Roentgenol Radium Ther Nucl Med 120:872,1974).We have not tried this but it is an interesting idea. Tumor seeding of the needle tract does not occur to any significant degree with the fine needle technique. This has been well documented in the literature, particularly by Nordenstrom and Bjork in a review of more than 4,000 cases (Nordenstrom B, Bjork VO: Letter to the editor. J Thorac Cardiovasc Surg 65:671, 1973). Our technique varies a little from that of Dr. Sagel’s group. We use a 22-gauge needle and pass it through an 18-gauge needle, which negotiates the skin and chest wall fasciae but does not reach the pleura. We limit the puncture to a single maneuver if we have good material. Most of the time there is nothing in the syringe, and the specimen is blown onto glass slides. We consider the pistol syringe very helpful: it produces a surprising vacuum and frees one hand (Camco Syringe Pistol, Precision Dynamics Corp, 3031 Thornton Ave, Burbank, CA 91504. Aspir-Gun, The Everest Co, 5 Sherman St, Linden, NJ 07036). Like Dr. Sagel’s group, we do not perform an aspiration needle biopsy on every potentially operable patient. A positive transthoracic needle biopsy, however, certainly expedites the procedure, for we don’t have to spend time doing a wedge biopsy or frozen sections. Instead, we can proceed immediately with the proper resection. The importance of a good cytopathologist cannot be overemphasized because a cytological diagnosis should be as good as a histological one, and most of the time a specific cell type should be identified. This is an important procedure that deserves more widespread use. DR. RICHARD M . PETERS (San Diego, CA): Before Dr. Jack Forrest came to San Diego from St. Louis, I was very skeptical of aspiration needle biopsy, but I must state that Dr. Forrest has convinced me that this procedure, as presented by Dr. Sagel, is a very important addition to the diagnostic armamentarium. It is far better for the patient when he can be told the diagnosis before operation. Also when we know we are dealing with carcinoma, not with possibly a granuloma, we are better able to decide whether to
405
Sage1 et al: Percutaneous Transthoracic Aspiration Needle Biopsy
proceed with operation in patients with very marginal function. Equally important, aspiration needle biopsy has saved a number of patients from an operative procedure. However, I would like to stress that it is extremely important not to accept the diagnosis of a negative biopsy. There must also be a histological diagnosis. It may be a granuloma or it may be some other infection, but, like a negative sputum, a negative needle biopsy has no meaning. Aspiration needle biopsy provides an easy and safe way for us to be much more specific in our therapy of patients.
how you achieve that. Invariably, we must wait 24 hours for an answer, while you implied that you take a biopsy specimen in the morning, receive an answer at lunchtime, and repeat a biopsy procedure in the afternoon. I would like a comment on that aspect of your procedure.
DR. THOMAS D. BARTLEY (Gainesville, FL): We, too, use aspiration needle biopsy of pulmonary lesions very aggressively and are very happy with the method. We practically never do a thoracotomy now without a previous positive histological diagnosis. I am interested that you are able to obtain sameday diagnosis from your pathologists, and I wonder
DR. SAGEL: The aspirated material for cytopathological study is placed in a tube containing a balanced electrolyte solution (Polysal) and conveyed to the pathology laboratory. Stained slides of the cytological preparation are available for interpretation within an hour. However, any available cell block would not be ready for at least 12 hours.
c . GRILLO (Boston, MA): A minor technical note. Dr. Reginald Greene, our pulmonary radiologist, reduced the incidence of pneumothorax markedly by using a two-needle technique. An outer needle is placed first in the target. Multiple aspirations are done by inserting a second needle through the outer one. DR. HERMES
