Transthoracic Needle Aspiration of Discrete PulInonary Lesions: Experience in 100 Cases ROBERT
w.
s.
FONTANA, M.D.
EUGENE MILLER, M.D.
JOHN W. BEABOUT, M.D. W. SPENCER PAYNE, M.D. EDGAR G. HARRISON, JR., M.D.
Needle aspiration of localized pulmonary lesions is not new: the procedure was first described almost a century ago. 6 • 7 Afterward, however, it fell into disfavor because of the cumbersomeness of radiologic equipment needed with it and because of concern over complications - especially pneumothorax, hemoptysis, and tumor dissemination. 8 Recently, interest in the technique has been reawakened by the introduction of sensitive image-amplification fluoroscopy and the development of cytologic methods having a high degree of diagnostic accuracy. It is now possible to direct needles of small caliber into very small pulmonary nodules with acceptable risk, as a number of published reports attest. 2 • 4. 9
MATERIAL AND METHODS We began performing transthoracic needle aspiration of circumscribed pulmonary lesions at the Mayo Clinic in early January 1968; Medical Clinics of North America- Vol. 54, No. 4, July, 1970
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and by May 1969 we had accumulated 100 cases, which form the basis for this report. The 100 patients ranged in age from 16 to 82 years with a median of 60 years. There were 64 patients between 50 and 70 years old, and the number of men also was 64. In each case, the needle aspiration was performed by a radiologist after consultation with a chest physician and a thoracic surgeon, each of whom had also reviewed the thoracic roentgenograms and the patient's clinical status. Pulmonary hypertension, hemorrhagic diathesis, anticoagulative medication, vascular lesions, and bullous changes within the region of lung to be aspirated were relative contraindications to the procedure. However, each potential case was evaluated individually.
Technique The aspirations were performed in the hospital radiology department. The patients lie on an image-intensification fluoroscopic table (the upright position was avoided because of the danger of air embolism).5 Premedication was usually unnecessary. The lung lesion was localized fluoroscopically and the overlying skin was marked. The skin was prepared with antiseptic solution and infiltrated with local anesthetic (1 % lidocaine). The anesthetic was then injected to a depth including the pleura. A small skin incision was made to minimize friction on the needle shaft, enabling one to feel the lesion more easily during biopsy. Although either a Fransen2 or a Cook1 needle could have been used for the procedure, we chose a standard thin-walled IS-gauge aortographic needle, 6 inches long, with all the bevel about its orifice sharpened. The needle was held with long forceps which allowed the radiologist's hands to be kept out of the fluoroscopic beam during biopsy. With the patient breathing quietly, the needle was advanced, under fluoroscopic control, until the lesion either was palpated or could be seen to move when impinged upon by the needle. Biplane fluoroscopy was often helpful but was not considered essential. Once a lesion had been entered, the stylet of the needle was withdrawn and a 30-ml Luer-Lok syringe was attached. Vigorous suction was applied while the needle was rotated within the lesion. The needle was then withdrawn with suction maintained. The specimen was smeared upon slides, which were quickly immersed in 70% alcohol solution to prevent cellular distortion from drying. These were stained with the Papanicolaou technique and screened cytologically. If a generous amount of material had been obtained, the larger clumps were visible on the slides; and these clumps were removed and processed in paraffin blocks and sections stained with hematoxylin and eosin or special stains, a procedure that enhanced the microscopic study. Also, if sufficient material were obtained, slides could be smeared for microbiologic staining. Meanwhile-just after the specimen had been taken from the needle - the needle and syringe had been rinsed in a vial of culture medium for microbiologic studies.
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The patient remained in the hospital overnight for observation, and inspiration and expiration chest roentgenograms were made the next morning for detection of pneumothorax. Then, if no adverse symptoms had developed, the patient was released.
RESULTS The indications for transthoracic needle aspiration among the 100 patients included in.our series are shown in Table 1. In 90 patients, the aspiration was done either to confirm a diagnosis of unresectable cancer or to establish a diagnosis of cancer in someone for whom thoracotomy would have been distinctly hazardous. Lesions obviously resectable were not needled unless surgical removal had already been declined by the patient or was deemed excessively risky. Our reason for refraining was concern over the possibility of seeding the needle tract with cancerous cells, despite assurances by others that this rarely occurs. 9 Similarly, because of fear of spreading infection, we attempted only a few aspirations of apparently inflammatory nodules. Moreover, we were reluctant to decide the disease was benign solely on the basis of a negative result of needle biopsy. Initially patients with obvious sizable peripheral pulmonary nodules were the only candidates accepted for needle aspiration. As our experience accumulated, however, it was found that smaller, more centrally located, and relatively inaccessible lesions could be biopsied safely and successfully. Because of the caliber of the aortographic needle used, bleeding from large blood vessels has not been a significant problem. Techniques have been refined to such a degree that a diagnosis of cancer has been confirmed by aspiration biopsy of a nodule less than 1 cm in diameter. Needle aspiration yielded cancer cells or fragments of cancerous tissue in 78% of the 83 cases of cancer involving the lung, but seemed of possible value in only 3 of the 7 cases wherein a diagnosis of benign disease was eventually confirmed (Table 2). Staphylococci were cultured from the needle aspirate in one of these three, and treatment with appropriate antibiotics was followed by disapTable 1. Indications for Transthoracic Needle Aspiration of the Lung in 100 Cases INDICATION
Suspected unresectable cancer Bilaterality Other contraindications Confirmation of resectable cancer Initial refusal of thoracotomy Increased operative risk Huge metastatic lesion Confirmation of benign disease
CASES
76
34
42 17 2
14
1
7
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Table 2.
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Diagnostic Accuracy of Transthoracic Needle Aspiration of the Lung in 100 Cases FINAL DECISION, CASES
DIAGNOSTIC CATEGORIES
Cancer Proved Strongly suspected Benign lesion, proved Indeterminate
81
2
83
7 10
AGREEMENT OF BIOPSY, CASES
65 (78%) 65
o
3 (?)
o
pearance of the pulmonary lesions. In the other two cases, the nodule that was biopsied imparted a marked sensation of resistance when transfixed by the tip of the aspirating needle. This has been described as typical of granulomas. In 10 patients, the precise diagnosis remains indeterminate as of this writing. Results of needle aspirations have been inconclusive, and more definite diagnostic data are lacking. Pneumothorax is by far the most common and most significant complication of needle aspiration of the lung. It occurred in 57 of the 100 patients in our series, as noted in Table 3. Aspiration of the pleural space by means of a malleable S-shaped needle or an intercostal tube was necessary in 1 7 cases, in 2 of which the complication was tension pneumothorax. The two instances of bilateral pneumothoraces occurred after simultaneous needle aspirations of both lungs, a practice we no longer follow. Though hemoptysis was noted in six cases, as a rule the amount of blood raised was slight. None of the other complications proved very serious. The one instance of transient aphasia and facial palsy occurred in a patient with known cerebrovascular insufficiency. There were no deaths among the 100 patients. Table 3. Complications of Transthoracic Needle Aspiration of the Lung in 100 cases None Pneumothorax Tension Bilateral Requiring intrapleural suction Hemoptysis Other Subcutaneous emphysema without pneumothorax Empyema Syncope, transient aphasia and facial palsy
34
2 2 17
57
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ILLUSTRATIVE CASES Three case histories will be summarized to illustrate some of the indications for, diagnostic benefits from, and complications of transthoracic needle aspiration. CASE 1. A 57-year-old woman underwent low-anterior resection of the rectum and sigmoidoproctostomy as treatment for carcinoma of the rectum. At the time of operation there was evidence of cancerous involvement of the peripheral fat and mesenteric lymph nodes. Then and 6 months afterward, thoracic roentgenograms showed no abnormality. However, a few months later another roentgenogram revealed multiple bilateral pulmonary nodules (Fig. 1). Studies of induced sputum specimens did not reveal cancer cells. Transthoracic needle aspiration of a nodule approximately 2 cm in diameter situated in the upper lobe of the right lung yielded fragments of well-differentiated adenocarcinoma consistent with metastasis from the original rectal lesion (Fig. 2). After the procedure a small pneumothorax developed (Fig. 3), but this did not require any treatment.
This case presents what may be regarded as the classic indication for transthoracic needle aspiration-namely, sizable and obviously
Figure 1 (case 1). Thorax, with multiple bilateral pulmonary nodules of metastatic adenocarcinoma from rectum.
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Figure 2 (case 1). Fragment of adenocarcinoma (metastatic from rectum) obtained by transthoracic needle aspiration (x600).
Figure 3 (case 1). needle aspiration.
Thorax, with small pneumothorax on right side after transthoracic
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unresectable bilateral peripheral nodules that almost certainly were metastatic carcinomas. An adequate sample of tumor tissue was obtained with only the minor complication of a small pneumothorax. CASE 2. A 61-year-old woman with hypercalcemia was found to have a tumor of the right superior parathyroid gland. This was resected, but the serum calcium concentration remained high. A preoperative thoracic roentgenogram had revealed multiple bilateral pulmonary nodules less than 1 cm in diameter (Fig. 4A). The exact nature of these nodules was not ascertained before surgery, but it was thought unlikely that they were metastatic neoplasms. Unfortunately, no prior roentgenograms were available for comparison. Specimens of induced sputum were negative for cancer cells, tubercle bacilli, and fungi. At an examination 3 months later, it was noted that the hypercalcemia persisted and also that the pulmonary nodules had enlarged slightly (Fig. 4B). Bilateral transthoracic needle aspirations were performed, one immediately after the other. Fragments of epithelial carcinoma were obtained that were considered consistent in appearance with metastatic cancer of the parathyroid.
Figure 4 (case 2). Thorax with bilateral pulmonary nodules of metastatic carcinoma from parathyroid- small in A, larger 3 months later in B.
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The aspirations produced pneumothoraces on both sides, with 40% collapse of the right lung and 10% collapse of the left (Fig. 5). The pneumothoraces were promptly corrected by suction applied via malleable S-shaped needles inserted into both pleural spaces.
In this case, needle aspiration not only elucidated the character of the pulmonary nodules but also explained the persistent hypercalcemia. The case serves to demonstrate that even very small pulmonary nodules can be biopsied with the help of image-intensification fluoroscopy. It also illustrates the potentially dangerous complication of bilateral pneumothorax that may occur if both lungs are aspirated at one time. This should never be done. CASE 3. A 64-year-old man was seen at the Mayo Clinic because of severe obstructive lung disease and diabetes mellitus, complicated by retinopathy, neuropathy, and arteriosclerosis obliterans. Roentgenographic examination disclosed a nodular density 1.2 cm in diameter located in the anterior segment of the left upper lobe. No calcification was demonstrable on tomography (Fig. 6). For obvious reasons, thoracotomy was thought inadvisable unless the lesion could be proved cancerous. Cytologic studies of sputum gave negative results, but needle aspiration of the nodule produced cancer cells of the large-cell type. Surgical exploration confirmed the diagnosis. The tumor was removed by a limited wedge-type resection.
Once again it is shown that fluoroscopy with image amplification may enable one to guide an aspirating needle into a very small lesion.
Figure 5 (case 2). Thorax after bilateral transthoracic needle aspiration, showing large pneumothorax on right side and smaller one on left.
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Figure 6 (case 3). Thoracic roentgenogram (above) and tomograms (below) of upper lobe of left lung, showing emphysematous changes and minute primary bronchogenic carcinoma without calcification.
In this particular case, the establishment of a definitive diagnosis of cancer tipped the balance toward surgical exploration when otherwise the risk of operation would have been considered prohibitive. COMMENT
We have found transthoracic needle aspiration of localized pulmonary lesions with guidance of image-amplification fluoroscopy a useful diagnostic procedure. As done with a small-bore needle in the manner described, it is not particularly uncomfortable and is generally well tolerated by the patient.
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The technique is fairly simple. Probably the most difficult aspect is the fluoroscopic guidance of the needle into the lesion. For this reason, the procedure is perhaps best performed by an experienced radiologist. We have tended to reserve transthoracic needle aspiration for cases in which simpler or more conventional tests either are not applicable or have yielded negative results. These tests include such standard diagnostic methods as cultures and cytologic studies of sputum (including study of induced sputum specimens), bronchoscopic examination, and scalene lymph-node biopsy. It is our opinion that the only acceptable candidates for needle biopsy are patients with indeterminate pulmonary lesions that would be unresectable if proved cancerous. Diagnostic thoracotomy is recommended for those patients with potentially resectable lesions, unless some contraindication exists. Transbronchial brushing3 and transbronchoscopic lung biopsyl may be carried out in selected cases as an alternative to thoracotomy. We believe these procedures are less likely to spread cancer or infection than is needle aspiration. By the use of transthoracic needle aspiration, we were able to establish the correct diagnosis in almost 80% of patients with cancer. This figure is in essential agreement with results reported by others. 2 , 4, 9 The diagnosis is primarily a cytologic one, but interpretation usually is not difficult for the pathologist experienced in pulmonary exfoliative cytology. On a number of occasions, we have been able to aspirate solid cores of cancerous tissue. However, even though we have tried several different types of needles,l° we have not consistently obtained cores of tissue. Therefore we have concentrated our efforts on improving techniques for capturing what few cells are present in the small biopsy sample. Recently we have been rinsing the biopsy needle and syringe with saline and then filtering that through a Millipore monitor filter. We hope this process will prevent loss of tiny tissue fragments. On the other hand (and in contrast to some6 ) we have been dissatisfied with fluoroscopically guided needle biopsy as an indicator of benign pulmonary disease. We have been unable to obtain a core of tissue from any benign lesion, alld a cytologic diagnosis of benign disease is often difficult. A microbiologic diagnosis may sometimes be substantiated by needle aspiration, but is not always reliable unless there is strong clinical support. We do not think prolonged observation of indeterminate localized lesions that might be resectable can be justified solely by a negative needle-biopsy finding. Under these circumstances, we would favor proceeding without delay to more definitive studies, including diagnostic thoracotomy if necessary. Pneumothorax, the only significant complication of guided transthoracic needle aspiration, developed in somewhat more than half of the patients in our series and was severe enough to require intrapleural suction in about one third of those in whom it occurred. In several instances the pneumothorax was not apparent immediately after the aspiration but became obvious and sometimes serious a number of hours later. This is why we prefer to keep all needle-aspiration patients
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under hospital surveillance at least until the day after the procedure. Then if respiratory distress is noted at any time, it can be evaluated and treatment begun promptly.
SUMMARY In aspirating localized pulmonary lesions in 100 patients by means of a small-caliber needle under fluoroscopic control, we found the technique simple, practical, and safe, provided there was no pulmonary hypertension, blood dyscrasia, or bullous emphysema. Lesions as small as 1 cm in diameter were aspirated successfully. Needle aspiration seems best suited for patients with presumably unresectable lesions or for those situations in which surgical resection has been refused or carries great risk. In our hands, the procedure has been most helpful in verifying the presence of cancer, where the diagnostic accuracy approached 80%. We have been considerably less enthusiastic about its value in the diagnosis of benign disease. The main complication of transthoracic needle aspiration of the lung was pneumothorax, which developed in the majority of patients studied. Hemoptysis was a less frequent and less serious complication. No specific treatment was needed in about two thirds of the instances of pneumothorax, but intrapleural suction was necessary in the remainder.
REFERENCES 1. Andersen, H. A., Fontana, R. S., and Harrison, E. G., Jr.: Transbronchoscopic lung biopsy in diffuse pulmonary disease. Dis Chest 48:187-192 (August) 1965. 2. Dahlgren, S., and Nordenstrom, B.: Transthoracic Needle Biopsy. Chicago, Year Book Medical Publishers, Inc., 1966, 132 pp. 3. Fennessy, J. J.: Bronchial brushing and transbronchial forceps biopsy in the diagnosis of pulmonary lesions. Dis Chest 53:377-389 (April) 1968. 4. Lalli, A. F., Naylor, B., and Whitehouse, W. M.: Aspiration biopsy of thoracic lesions. Thorax 22 :404-407 (Sept.) 1967. 5. Lauby, V. W., Burnett, W. E., Rosemond, G. P., and Tyson, R. R.: Value and risk of biopsy of pulmonary lesions by needle aspiration: Twenty-one years' experience. J Thorac Cardiov Surg 49:159-172 (Jan.) 1965. 6. Leyden, H.: Uber infectiose Pneumonie. Deutsch Med Wschr 9:52-54, 1883. 7. Menetrier, P.: Cancer primitif du poumon. Bull Soc Anat Paris 61 :643-647, 1886. 8. Ochsner, A. and DeBakey, M.: Primary carcinoma of the lung. New Orleans Med Surg J 93:387-394 (Feb.) 1941. 9. Stevens, G. M., Weigen, J. F., and Lillington, G. A.: Needle aspiration biopsy of localized pulmonary lesions with amplified fluoroscopic guidance. Amer J Roentgen 103:561-571 (July) 1968. 10. Turner, A. F., and Sargent, E. N.: Percutaneous pulmonary needle biopsy-an improved needle for a simple direct method of diagnosis. Amer J Roentgen 104: 846-850 (Dec.) 1968.