Percutaneous aspiration biopsy of nodular lung lesions Over a 24 month period, 39 patients with nodular lung lesions suspected of being malignant on chest x-ray study underwent transthoracic needle aspiration biopsy. An accuracy rate of nearly 100 per cent was obtained in 34 of the lesions subsequently proved to be malignant. Achieving these results requires very close cooperation between the departments of radiology, cardiology, and cytopathology.
Jack E. Meyer, M . D . , * Lalita H. Gandbhir, M.D.,** Lee B. Milner, M.D.,*** and Margaret M. McLaughlin, C.T. (ASCP),**** Walpole and Boston, Mass.
JL ercutaneous aspiration biopsy of undiagnosed lung lesions is now an accepted procedure of high diagnostic yield which can be performed in a short period of time with very little risk to the patient. 1-3 The indications for and performance of this procedure, however, are sometimes poorly understood. Our department of radiology has been asked to re-examine biopsy specimens presumed benign because of negative results from aspirations at other hospitals which were attempted without fluoroscopic control or proper cytologic handling. Because of the heretofore unreported high rate of accuracy attained in this study, we believe that re-emphasis of the technique and its proper use is indicated. In 1973, a joint study was instituted by the pathology and radiology departments to improve lung biopsy results and widen the spectrum of lesions which could be evaluated with the percutaneous biopsy technique. Previously, only core biopsies with the Vim-Silverman needle were performed, and only larger lesions located From the Commonwealth of Massachusetts, Department of Public Health, and the Pondville Hospital, Departments of Radiology and Pathology, Walpole, Mass. 02081. Received for publication Oct. 7, 1976. Accepted for publication Nov. 29, 1976. ♦Assistant Professor of Radiology, University of Massachusetts Medical School; Associate Clinical Professor of Radiology, Boston University School of Medicine; Chief of Diagnostic Radiology, Pondville Hospital, Box 111, Walpole, Mass. 02081. **Chief of Pathology, Pondville Hospital, Walpole, Mass. ♦"Instructor in Radiology, Boston University School of Medicine, Boston, Mass. ****Cyto-Technologist, Pondville Hospital, Walpole, Mass.
in the lung periphery or pleura were considered for biopsy. Needle aspiration is not a core biopsy, but a cellular sampling, and allows a safer evaluation of a much broader range of lung lesions. We have also utilized the bronchial brushing technique in the evaluation of lung lesions, especially undiagnosed infiltrates; however, as others have reported, this method is not as accurate as aspiration, especially in metastatic lesions or smaller, peripherally located primary lung carcinomas.3 Indications for lung aspiration include (1) lesions suspected of being malignant but not proved to be so by clinical or laboratory evaluation; (2) confirmation of the presence of lung metastases in patients with known malignant lesions; and (3) bacteriologic evaluation of inflammatory lung lesions. All types of lesions of the lung, bone, subcutaneous tissue, and breast have been aspirated with equal accuracy, but this review pertains only to solitary or multiple lung nodules. All lung lesions except those close to the heart or hila were considered for biopsy. Hilar and mediastinal lesions were not studied in this series; however, a technique for evaluation of these areas has been described.4 In patients with severe chronic obstructive pulmonary disease or low platelet counts or those who require anticoagulation, the risk of biopsy should be weighed against the potential value of the information obtained. It is essential that the patient be able to cough and to suspend respirations on command. Normal results from cytologic study of the sputum plus laminographic and fluoroscopic studies are the minimum prebiopsy work-up for small, peripherally located lesions less than 2.0 cm. Depending on the 787
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Fig. 1. Clinical diagnosis: Primary lung carcinoma. Cytologic diagnosis: Undifferentiated carcinoma. (Cell block; original magnification x43.)
Fig. 2. Clinical diagnosis: Primary lung carcinoma. Cytologic diagnosis: Poorly differentiated epidermoid carcinoma. (Cell block; original magnification x43.)
clinical circumstances, patients with a larger, more centrally located density should have a complete work-up including a bronchoscopic and possibly mediastinoscopic examination before consideration for lung biopsy.
anesthesia infiltration is applied to the periosteum of the adjacent superior rib margin and pleura. A 6 or 8 inch, 19 gauge spinal needle with a stylette is inserted (18 or 20 gauge needles are just as satisfactory) while the patient suspends respirations. The needle is passed over the superior rib border to the estimated depth into the lung. Usually, a slight resistance is noted as the lesion is entered. The stylette is then withdrawn, a 10 cc. disposable plastic syringe rinsed with saline is attached, and negative pressure is applied as the needle is advanced slightly and then withdrawn. The needle and syringe are given to the cytologist who immediately prepares the slides in the radiology department. Reexamination with the fluoroscope to check for a pneumothorax is then performed and often reveals a slight increase in density in the lesion, which is probably the result of some minimal hemorrhage. A posteroanterior chest x-ray film is taken immediately and 3 hours after the procedure. Initially, two to three aspirations were made at each sitting, but subsequently
Method A C-arm or biplane fluoroscope is not necessary to perform this procedure. Single-plane image intensification with a television monitor was utilized for this study and is available in most x-ray departments. The patient is positioned either prone or supine, depending on the location of the lesion. Oblique positioning is rarely necessary and may be a cause for error. Careful localization of the lesion with the aid of the fluoroscope is necessary to determine the site of skin entry. The needle must be directed parallel to the x-ray beam and perpendicular to the floor, except in lesions in the lung apex, in which oblique angulation of the needle may be necessary.5 After the skin is prepared and draped, local
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Fig. 3. Clinical diagnosis: Myxosarcoma metastatic to the lung. Cytologic diagnosis: Sarcoma cells present. (Cell block: original magnification x43.)
only one was made, as confidence developed in both performance and interpretation. A single aspiration was performed in the evaluation of the most recent 20 patients, with one exception when the procedure was repeated the following day. Patients The range in size of the lesions aspirated was 5 mm. to 9 cm. with an average of 3.9 cm. The age range of the patients was between 30 and 81 years with a mean of 63 years. All patients had normal results from prebiopsy sputum examination, 24 of 39 had normal findings from bronchoscopic studies, and 12 of 39 had normal results from both bronchoscopic studies and scalene node biopsies. Four patients had previous aspiration biopsies at other hospitals, the results of which were normal. Only in those patients with small, peripherally located lesions was it believed unneces-
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Fig. 4. Clinical diagnosis: Endometrial carcinoma metastatic to the lung. Cytologic diagnosis: Papillary adenocarcinoma consistent with endometrial primary lesion. (Cell block; original magnification x43.)
sary to do a preliminary bronchoscopic study because of the low yield. Results Thirty-nine patients were studied over a 24 month period. Thirty-four lesions were proved malignant surgically, clinically, or at autopsy. Aspiration had indicated malignancy in 33 of these 34 cases, for an overall accuracy rate of 97 per cent. In the other lesion, malignancy was suspected from examination of the aspirate. In one patient with normal biopsy results, the lesion was benign at operation. Four others have had evidence of a benign process on follow-up radiograms. Complications Fourteen (35.9 per cent) of the patients had a pneumothorax, 4 of whom required a chest tube (10.2
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Fig. 5. Clinical diagnosis: Breast carcinoma metastatic to the lung. Cytologic diagnosis: undifferentiated tumor cells in a pattern consistent with primary breast lesion. (Cell block; original magnification x43.) per cent). Transient hemoptysis occurred in 3 of 39 (7.6 per cent). No other problems were encountered, and there were no instances of needle track tumor implantation. Pathology The cellular sample is small and must be processed immediately to avoid drying. The cytologist was always present during the procedure. Technique Smears. Material from the syringe is expelled onto plain slides, smeared, and fixed with a spray fixative. The specimens are then stained by the standard Papanicolaou technique. Cell block. Bouin's solution (2 c.c.) is drawn through die needle into the syringe, transferred to a small test tube, and centrifuged at a rate of 2,000 r.p.m. for 5 minutes. The supernatant is aspirated and discarded. A few drops of warm liquid nutrient agar (6.5 per cent) are added to the sediment.6 The agar
button is quickly poured on filter paper and flattened, fixed in 10 per cent formalin, and processed as a cell block. The yellow color of Bouin's solution is helpful in locating the specimen in the paraffin cell block. The speciman is step sectioned and stained with routine hematoxylin and eosin technique. Special stains may be done. Smears were made on all biopsy specimens and indicated malignancy in 33 of 34 lesions subsequently proved to be malignant. Of the 34 patients with proved malignant tumors, 27 had cell blocks positive for tumor cells; of these, 17 had minute tissue fragments or minute biopsy specimens in which the characteristic histologic type was identifiable. Ten cell blocks had minute clusters of tumor cells. Of the malignant lesions, 25 were histogically typed or classified. Histologic follow-up on tissue from surgical or autopsy specimens was available in 16 cases, and all but one was typed correcdy. Of those classified correcdy, seven were from primary lung carcinomas and included three undifferentiated carcinomas (Fig. 1), one adenocarcinoma, and three epidermoid carcinomas (Fig. 2). Included in eight metastatic tumors to the lung were two melanomas, two adenocarcinomas of the colon, one myxosarcoma from the thigh (Fig. 3), one endometrial carcinoma (Fig. 4), one breast carcinoma (Fig. 5), and one carcinoma of die kidney. One biopsy specimen typed as undifferentiated carcinoma was signed out at autopsy as well-differentiated squamous cell carcinoma with areas of adenocarcinoma. Cell blocks did not yield positive results as often as smears: however, they were very helpful in histologic typing because architecture is visible in minute tissue fragments. Others have also commented on this fact. 7,8 As the smear is direcdy from aspirated material, very litde search for tumor cells is necessary unless a large amount of necrotic material is aspirated. As compared to exfoliated cells, these cells appear morphologically better preserved,7- 9 and attempts have been made to compare the structure of exfoliated cells with that of cells obtained by needle aspiration biopsy of me lung.910 Other cells found in smears are histiocytes, columnar cells, leukocytes, and red cells. Because of the aspiration biopsy technique, smears on a whole new set of tumors rarely seen in exfoliative cytologic studies are being obtained, such as myxosarcoma, melanoma, and carcinoma of the colon. Discussion The key to obtaining a near 100 per cent accuracy rate with the aspiration biopsy technique lies in careful fluoroscopic localization as well as rapid, meticulous
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cytologic handling. It is difficult for the person performing the aspiration to attempt to prepare the slides or to send the material to the pathology department. It is noteworthy that even though there is a significant risk (35.9 per cent) of pneumothorax, 25 per cent of the biopsies were performed on an outpatient basis without any complications. The patients stay in the hospital outpatient department for 3 hours after the procedure, and repeat frontal chest x-ray films in inspiration and expiration are taken. If no pneumothorax is present, the patient is sent home with precautions and returns the following morning for a final chest x-ray film. Results are available within 24 hours of the procedure, not only with a diagnosis of malignancy, but in more than 60 per cent of cases with an indication of cellular origin. If necessary, smears may be stained and interpreted in 2 hours. This information may avoid or at least shorten a hospital stay and any number of more complicated, time-consuming diagnostic procedures. In all but one patient the information obtained prompted further treatment, i.e., surgery, radiotherapy, or chemotherapy. REFERENCES 1 Dahlgren, S. E., and Nordenstrom, B.: Transthoracic Needle Biopsy Uppsala, 1966, Almquist and Wiksell, Gebers Forlag. 2 Lalli, A. F., Naylor, B., and Whitehouse, W. M. Aspiration Biopsy of Thoracic Lesions, Thorax 22: 404, 1967.
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3 Landman, S., Burgener, F., and Lim, G.: Comparison of Bronchial Brushing and Percutaneous Needle Aspiration Biopsy in Diagnosis of Malignant Lung Lesions, Radiology 115: 275, 1975. 4 Jereb, M., and Sinner, W.: The Use of Some Special Radiologic Procedures in Chest Disease, Radiol. Clin. North Am. 11: 109, 1973. 5 Walls, W. J., Thornbury, J. F., and Naylor, B.: Pulmonary Needle Aspiration Biopsy in Diagnosis of Pancoast Tumors, Radiology 111: 99, 1974. 6 Shackelford, R. I., and Jones, J. L.: An Embeding Medium for Permanent Sections of Exudative Material and Fragments of Tissue Removed for Biopsy. Technical Bulletin of the Registry of Medical Technology, 29: 155, 1959. 7 King, E. B., and Russell, W. M.: Needle Aspiration Biopsy of the Lung: Technique and Cytologic Morphology, Acta Cytol. 11: 319, 1967. 8 Pavy, R. D., Antic, R., and Begley, M.: Percutaneous Aspiration Biopsy of Discrete Lung Lesions, Cancer 34: 2109, 1974. 9 Magnas, N.: Diagnosis of Lung Cancer by Aspiration Biopsy and a Comparison Between This Method and Exfoliative Cytology, Acta Cytol. 11: 114, 1967. 10 Yoshihior, H., Oho, K., Tchiba, M., Goya, T., and Hayashi, T.: Percutaneous Pulmonary Puncture for Cytologic Diagnosis: Its Diagnostic Value for Small Peripheral Pulmonary Carcinoma, Acta Cytol. 17: 469, 1973.