Biopsy of the Lung* I~OBERT W;. JAMPLIS, M.D., G. MELVIN STEVENS, GLEN A. LILLINGTON, M.D.,
Fuon~ tks~ I)eputbwnfs
REPORT T HIS percutaneous localized
fier fluoroscopy believe
of the needle.
this to be a most direct inexpensive.
is fraught and
undue sequelae. to spread suspected operate
should be carried
be the case
out on an out-
in the hospital
or who were too ill to be
preparation it is not
of the patient necessary
tion that affords the most ready access to the lesion. The imprint of a metallic marker in the
on the fluoroscopic
table in a posi-
skin is used as the site of entry after
the patient; disease; (4)
refusal of thoracotomy by confirmation of metastatic presence
cyst out in
seen in the clinic.
one would not want
cases. Also, if the patient
INDICATIONS AND CONTRAINDICATIONS present
yields poor diagnostic the needle
If one could
of an echinococcal
for any reason,
should not be carried
indeed not founded in fact.
was of vascular
and needle biopsy
the needle has traversed
with a high degree of
with this method,
it might be well to avoid puncturing
to the interest
ence of the investigator.
or any other medical endeavor,
sis or severe
of even small and cen-
as in cytology directly
It has greatly
in the diagnosis
would include such things as a bleeding
lesions using image ampli-
one which is safe, essentially tively
Prrlo Allfo, Cn&foornicl
and ;Il~~dic-ul(‘best Diseases, Palo Alto Clinir and Stanford I~niwrsit_~ S‘tkool of Medicine, Palo Alto, CaliIovnia.
The skin is then painted
out for any persistent
of the needle
with an anti-
anesthetic marked and
care being taken to avoid the intercostal nerve and vessels. A tiny nick is made through the
lesion of the lung which
at the Thirty-Ninth Annual Meeting of the Pacific Coast Surgical Association, Honolulu, Hawaii, February IX-E, 1968. 243
1 2 FIG. 1. Technic employing balsa wood handle for guidance of 6 inch n-0. 18 gauge aortogram needle usi:lg image amplifier fluoroscopy. FIG. 2. The needle tip has been placed in the pulmonary lesion with the patient under local anesthesia and suction is being applied to the syringe to obtain the needle aspiration biopsy.
skin with a pointed blade to prevent skin fragments from entering the needle. Ordinary 3 and 6 inch No. 18 gauge thinwalled aortogram needles with the standard bevel are used. They are easily guided and have the proper flexibility. Since the needle is introduced under direct fluoroscopic control it is necessary to keep radiopaque objects, such as lead gloves, from the field. Therefore, two 8 inch pieces of balsa wood have been fashioned and serve well as a radiolucent needle holder. They are mirror images of each other and so constructed as to conform to the shape of the needle hub at their opposing faces. They can be separated easily once the needle has been properly placed in the lesion, but give firm control during the placement. (Fig. 1.) The needle is introduced with the stylet in place while the patient’s respiration is suspended. Then, when exact localization of depth is determined, the patient is allowed to breathe quietly. Several criteria are used to be sure the needle tip is impaled in the lesion and this final placement is carried out with the bare hand so as to get the “feel.” Sometimes an increased resistance can be felt as the needle enters the tumor. Also by gentle manipulation of the needle hub, the lesion itself can actually be moved. Furthermore, if during respiratory excursions the needle tip and the lesion are always superimposed, they must be in contact with one another. However, if the lesion is small, or if it is in a relatively immobile portion of the lung, such as the hilum or apex, other
determinations must be made. One can utilize the principle of parallax by opening the fluoroscopic shutters wide and circling the needle hub. If the needle tip stays within the lesion at all times, it is correctly placed. Another method is to take tomograms with the patient in the desired biopsy position. Then, by subtracting the distance from the top of the table to the lesion from the caliper-measured tabletopneedle entry site, one knows the approximate depth that the needle must penetrate. Rotating the patient himself can help but has the disadvantage of dislodging the needle. All of this can be obviated by using a Cordis Rotocor or biplane or “C” arm image amplifiers, but these are not essential to the procedure. Once the operator is satisfied with the placement of the needle, the stylet is removed and a 20 cc. Luer-Lok’ syringe, pretested for tight suction, is attached to the needle hub. While vigorous suction is applied constantly to the syring, the needle is rotated and several short “in and out” penetrations of the lesion are made. (Fig. 2.) The needle is then withdrawn while suction is maintained. How the specimen is handled at this point is as vital to success as guiding the needle to the tumor. Enough material for pathologic and bacteriologic examination, as well as occasional special staining is desired. Cytologic preparations are made by placing several drops of fluid from the needle on slides and immersing them in alcohol; they should not be smeared as this tends to distort the cells. A few other drops are The American
Jouvnal of Surgery
Needle Aspiration Biopsy of Lung
with the number of biopsies performed. Table is a compilation of the results obtained. Confirination of the accuracy of diagnoses oi benign and malignant lesions was determined by study of the surgical and autopsy specimens, results of cultures, the clinical course of the patient, and radiographic findings. Sixty-two lesions were proved to be malignant and thirty-eight to be benign. This represents a diagnostic accuracy in malignant lesions of S4 per cent and in benign lesions of i9 per cent. _Ytl accurate distinction between malignant and benign disease was either established or suspected in 92 per cent of the cases. I
Frc,. 3. l’llotolnicrograph of tissue from a bronchogenic small crll carcinoma obtained from a percutaneous needle :r\p1ratlcn~ biopsy of the lung.
placed on slicles and smeared and stained for routine pathogens, acid-fast bacilli, fungi, and other tissue or organisms, depending on the nature of the disease. Other drops are placed in sterile tubes for aerobic and anerobic cultures. Then several cubic centimeters of Bouin’s solution (formaldehyde and picric acid) are aspirated through the needle and into the syringe to capture any and all small tissue fragments sticking to the inside of the needle and to the wall of the syringe. This is then ejected back into the Bouin’s solution and allowed to stand for about three hours. It is then spun down and a cell button prepared for histologic section. The remaining solution is further passed through a Millipore filter and in this way practically all cells are retrieved for study and excellent preparations are obtained. (Fig. 3.) After the needle is withdrawn, an anteroposterior roentgenogram of the chest with the patient in expiration is taken immediately. The patient is observed closely for any untoward reactions and in one hour the same type of film is taken again. If no complications have occurred, the patient is allowed to leave the x-ray department with instructions to return the next day for a final film. RESULTS
separate procedures with a total of 192 biopsies carried out on 100 indeterminate localized pulmonary lesions over a three year period. Seventeen patients had two procedures and six had three procedures Just as in the case with cytology, the percentage of definite diagnoses arrived at increases There
There were no deaths and complications were few if one discounts mild, self-limiting pneumothoraxes or hemoptysis. There were thirtynine instances of pneumothorax after 126 needle aspiration biopsy procedures giving an incidence of 31 per cent. Most were small, asymptomatic, and resolved spontaneously. In nine patients, although most were asymptomatic, we resorted to several days of closed intercostal drainage, mainly because of our belief that any pneumothorax greater than 10 per cent should be treated aggressively in that fashion. Eight of these nine patients had had two or more biopsies during the same procedure. For that reason we now believe that only one biopsy should be carried out during a single procedure.
TABLE I DIAGNOSTIC ACCURACY OF NEEDLE I3IOPSY IS ONE HUNDRED LOCALIZED LESIONS Result ____
of Needle Biopsy __ ~_____
No. of Lesions ~
Lesions proved mnkgnanl Malignant Malignancy suspected (three by surgery) Nonmalignant (false-negative! Total
proven 1 f, 6%
Lesions proved benip Specific organism cultured Benign neoplasm Granuloma Infected cyst or abscess Miscellaneous infection Benign but nonspecific disease Malignancy diagnosed (false-positive Total
7 4 7 4 r, 0
A B FIG. 4. Anaplastic bronchogenic carcinoma of the left upper lobe with hilar involvement. Diagnosis was made by needle aspiration biopsy and left pneumonectomy was performed six weeks after completion of supravoltage irradiation. A, preirradiation on December 22, 1967; B, postirradiation on February 24, 1967.
The entire procedure can then be repeated at a later time with less danger of pneumothorax. Sputum was blood-tinged in six patients for only a matter of minutes, and there was no incidence of massive hemorrhage. One patient had transitory hypotension and another had a small hemopneumothorax. Of great significance is the fact that there has been no evidence to date suggesting tumor implants along the needle tracts, nor has there been spread of any infectious process. Also we have encountered no air embolism. COMMENTS
Leyden [I] in 1883 was the first to describe the use of percutaneous needle aspiration biopsy in the diagnosis of an infective process in the lung. Menetrier  employed the same technic three years later in confirming the diagnosis of bronchogenic carcinoma. The procedure was not utilized for the next fifty years, but then scattered reports began to appear in the literature [3-131. At the beginning of this decade the technic seemed to be gaining favor and various investigators began to experiment with different types of needles for both diffuse and localized pulmonary lesions [I4-191; it soon became obvious that needle aspiration biopsy should be confined to the localized type. Bigger pieces of tissue are necessary to diagnose the more diffuse diseases. Aronovitch et al. [ZO] stressed the reliability of needle aspiration biopsy in the diagnostic armamentarium of the
thoracic physician, but real impetus was given to the procedure by a paper appearing in 1965 by Lauby et al. [2I] in which they reported their results with an extensive series of cases followed up for a long period of time. Authors of other reports in the last two years [22-261 have been enthusiastic in endorsing the method, but by far the greatest experience is that of Dahlgren and Nordenstrom  in Sweden who have biopsied many hundreds of lesions. They have emphasized the use of small caliber needles which are guided by image amplifier fluoroscopy. Combining all of the references previously cited, well over one thousand malignant lesions have been biopsied, with only two instances of tumor-seeding along the needle tract being reported [4,20]. This does not include pleural mesotheliomas, which notoriously spread in that fashion and for this reason needle biopsy should not be used if this lesion is suspected. Of the total of more than 2,700 cases in which biopsy was carried out, there were six fatalities (0.2 per cent). Two were from hemorrhage w221, one from a tension pneumothorax , and one from air embolism . Two other deaths were probably not related to the biopsy [ZI ]. Lauby and his group have advocated the use of the needle biopsy when the conventional diagnostic methods have failed. We believe it should not be used as a last resort, but rather that it should be carried out soon after sputum The American
PIG. XI and IS. Bronchogcnic small cell carcinoma of the left lung was diagnosed by needle aspiration hlol+)-. patiwt, who was elderly and had severe aortic stenosis, was given cobalt irradiation. Diagnostic thorac,,t
examinations (if these give negative results) and concomitant with bronchoscopy and scalene fat pad biopsy, which are still essential even if a tissue diagnosis has already been established. For the past five years we have been using preoperative supravoltage irradiation according to a protocol schedule in all cases of bronchogenic carcinoma other than those presenting as peripheral coin lesions. It is too early to evaluate the efficacy of this approach, except to note that many more lesions are resectable. Whether or not the cure rate will also rise remains to be seen. However, for those surgeons following such a regime, the needle aspiration biopsy technic becomes all important since it is preferable that a definite diagnosis be determined short of exploratory thoracotomy. (Fig. 3, 5 and 6.) It should also be pointed out that when the needle biopsy and other tests are inconclusive and no definite diagnosis can be entertained, then the lesion is considered to be an indeterminate one and we proceed directly to diagnostic thoracotomy. Six biopsies gave falsenegative results in our series and the lesions lvere subsequently proved to be malignant at operation. Therefore, although we believe that this procedure has great merit, it is by no means foolproof. In this respect it can be likened to mammography in detecting carcinoma of the breast: A positive report is important lvhereas a negative one is of little value. However, as in mammography, it is of great benefit
1 hta 1~x5
to the surgeon in planning the management of a particular case. Several of the patients have initially refused thoracotomy, but \vhen the needle biopsy proved the lesion to be malignant, they became anxious and agreed to surgery. Finally a word concerning the role of needle aspiration biopsy in peripheral coin lesions is in order. Since we do not irradiate these lesions preoperatively, one might question the rationale of a needle biopsy. However. if a malignant lesion is discovered, one can proceed directly with the lobectomy without a \vedge biopsy.
FIG. 6. Bilateral alveolar cell carcinoma of the !u~li: was diagnosed by needle aspiration biopsy. therrby Jvoiding diagnostic thoractomy.
FIG. 7. Central
coin lesion of the right lung diagnosed on needle aspiration biopsy to be active tuberculosis on smear and culture. Patient responded well to chemotherapy.
We believe the needle biopsy will create less trauma and less potential tumor dissemination than will the open biopsy. Furthermore, we used to state that the presence of the lesion unchanged from that seen on films taken seven years previously or dense laminated calcium in the lesion itself were the only things that would eliminate thoracotomy. However, by needle aspiration we have diagnosed active infections such as tuberculosis (Fig. 7), coccidioidomycosis, and cryptocococcis, which have cleared on medical management. Hamartomas have even been diagnosed with certainty since no other pulmonary tumor contains cartilage. We still elect to remove these in an otherwise healthy patient. SUMMARY
Localized pulmonary disease can be safely and accurately diagnosed by means of percutaneous needle aspiration biopsy using image amplifier fluoroscopy for guidance of the needle. This is true whether the lesion is large or small, central or peripheral, or benign or malignant. It is usually performed on an outpatient basis in the x-ray department with local anesthesia being used so that little or no pain will be experienced by the patient. Simple 3 to 6 inch 18 gauge needles holding a stylet are used and
the aspirant is sent to the laboratory for cytologic and bacteriologic examination. The procedure is particularly useful for those surgeons using preoperative irradiation in bronchogenic carcinoma since it gives a higher diagnostic yield than any other test short of thoracotomy. Other indications for its use include medical contraindication to or patient refusal of thoracotomy; the presence of metastatic, bilateral, or inoperable disease; unresolved “pneumonia;” and any persistent indeterminate localized lesion which cannot be diagnosed by other means. There were 192 biopsies performed on 100 lesions. Sixty-two of the lesions later proved to be malignant. In this latter group there was an 84 per cent rate of diagnostic accuracy using the needle biopsy technic. False-positive results occurred in 2 per cent and false-negative in 6 per cent. The latter were treated as indeterminate lesions and these patients were operated upon. There were no deaths and no serious complications. Biopsy of 31 per cent of the lesions resulted in pneumothoraxes but in only 7 per cent was closed intercostal drainage required. Six per cent of the patients had brief mild hemoptyses but no alarming bleeding. There was no evidence of tumor dissemination along The American
Needle the needle embolism.
1. LEYDEN. H. Uber infcctiose Pneumonic. Del&-c/z nzed. Il~schnsYhv., 9: 52, 1883. L’. MENETRIEK, P. Cancer primitif du poumon. B&1. Ser. nnclt. Paris, 11: 613, 1886. 3. CRAVER, L. F. and BINKLEY, J. S. Aspiration biopsy of tumors of lung. J. Thovacic Szlrg., 8: 436, 1939. 4. DCTRA, F. R. aud GERACI, C. L. Seedle biopsy of the lung. J..l ,V..l., 155: 21, 1954. .i. FKANSEEN, C. C. .xspiration biopsy with a description of a new type of needle. Neze, E~zgland J. .lfed. “24: 105-I 1931. (i. GI.EDH& E. <‘.: SPRIGGS, J. B., and BINFORD, C. II. Needle aspiration in the diagnosis of lung carcinoma; report of experience with 75 aspirations. .1~2. J. Clint. Path., 19: 235, 1949. 7. MARTIN, H. E. and ELLIS, E. B. Aspiration biopsy, Sure. Gvnec. &Y Obst.. 59: 578. 1934. Y. MAR&, k. E. and STEWART, F. W. Advantages and limitations of aspiration biopsy. Am. J. Koentgenol.. 35: 245, 1936. 9. MILLER, F. L. Percutaneous needle biopsy in clinically inoperable pulmonary tumors. C’. S. .Armed Forces Xed. J., 11: 858, 1960. 10. ROSEMOSD. G. P., BURNETT, W. E., and HALL, J. H. Value and limitations of aspiration biopsy of lung lesions. Ku&logy, 52: 506, 1949. 11. SAPPINGTON, S. W. and FAVORITE, G. 0. Lung puncture in lobar pneumonia. Am. J. X. Sci., 191: 225, 1936. 1%. VAN ORDSTRAND, H. S. and LAMBERT, T. H. The value of aspiration biopsy in diagnosis: with illustrative cases. Clereland Clin. Quart., 8: 175, 1941. 13. WOOLF, C. R. .Ipplications of aspiration lung biopsy with a review of the literature. Dis. Chest, “5: 286, 1954. 14. HAUHER, R. Uber die diagnostische gezielte Gewebspunktion bei Unklaren Lungen-Pleura und Medidstinalprazessen. n&s&e sled. Il.&nsc-hr.. 90: 1809, 1965. (English synopsis published in abstract form in J.A.x.A., 194: 217, 1965.) 15. MANFREDI, F., ROSENBAUM, D., and BEHNKE, R. H. Percutaneous needle biopsy of the lung in diffuse pulmonary diseases. Ann. Int. Med., 58: 773, 1963. 16. MANFREDI, F. and KRUMHOLZ, R. Percutaneous needle biopsy of the lung in evaluation of pulmonary disorders. J..-I M.A _, 198: 1198, 1966. li. SAHOUR, M. S., OSMAN, L. M., LE GOLVAX, P. C., AND ISIIAK, I(. G. Needle biopsy of the lung. Lnnc-et, 2: 182, 1960. 18. SCHIESSLE, W. and KONS, G. La ponction-biopsie transparietale du poumon et du mediastin. Technique et resultats. J. franc. mtd. et chir. thornc-., 19: 593, 1965. 19. S~~ITH, W. G. iYeedle biopsy of the lung. With special reference to diffuse lung disease and the use of a new needle. Z%ornr, 19: 68, 1964. 20. >\RONOVITCH,M., CHARTIER, J., KAHANA, L. M.,
~I~AKISS, J. F.. and GROSZE~IAS,hl. Seedle biopsy as an aid to the precise diagnosis of intrathoracic disease. Qlnczd. JI. _-I. J., ?i8: 120, 1963. LAURY, V. W., BURNETT, W. E., ROSE&~(ISD, G. P., and Tssos, K. K. f:;tluc anti risk of biopsy of pulmonary lesions by needle aspiration. J. Thorac-ic. $ Ca:nrdim~sc:..Curg., 49: 150, 191X ADAMSOS, J. S., Jr<. and BATES, J. II. Percutaneous needle biopsy of the lung. drch Int. MN!., 119: 164, 196;. KRUMHOLZ, R. .\. and WEG, J. G. Pcrcutaueous needle biopsy of the lung. .1..l..l,f ,l,( 195: 38, 1966. LALLI, A. F. Technique for lu:lg tumor diagnosis. J./l Bf.d ., 1967. hbwN, B. and SINHA, C. S. Jack needle lung biopsy in pneumoconiosis. TI;s. C/zest, ,50: 501, 1966. STEVESS, G. M., LILI.INGTON, G. A., and WEIGEX, J. F. Needle aspiration biopsy of localized pulmonary lesions. G~li~~unin Xed., 106: 92, 1967. DAHLGREN, S. aud SORDENSTROM, B. Transthoracic Seedle Biopsy. Chicago, 1966. Ye:ir Bocjk Publishers. DISCUSSION
JOHN E. CONNOLLY (Irvine, Calif.): If needle biopsy is to be substituted by the medical staff for the extensive prolonged work-up that is currently so common I could perhaps accede to its routine use as recommended by Dr. Jamplis and his associates. I believe that many thoracic surgeons completely eliminate the possibility of needle biopsy because they have a false opinion of the rate and severity of complications. We teach our residents to employ needle biopsy in a number of instances: (1) in poor risk patients; (2) in apparently nonresectable lesions; (3) when there is evidence of metastatic spread; and (-1) when one believes that preoperative radiation may be indicated. I would agree that tumor spread and pneumothorax are probably not serious problems, but I would maintain that needle biopsy in the patient with an operative, isolated, indeterminate lesion does not unequivocally change our plans. If it is proved malignant, we operate; if it is proved [email protected]
it is still necessary to operate to be absolutelv certain. In this type of circumscribed lesion I he&e that needle biopsy is unnecessary and ma)- even be meddlesome. WALTER F. MERDINCER (La Jolla, Calif.): We employ the Silverman needle biopsy with no greater complications than were described by Dr. Jamplis. We have used this not onlv for localized lesion but also for the bilateral dens&s one sees in the Hamman-Rich syndrome. We had one rather frightening experience in a debilitated elderly woman in whom needle biopsy was carried out for the Hamman-Rich syndrome. After biopsy was performed, massive hemoptysis occurred. WC now place a plastic needle in a vcln in these patients and insure the ready
Jamplis, Stevens, and Lillington
availability of cross-matched blood so that we are not unprepared if massive hemoptysis should occur. We still believe that the complication rate is far lower than the morbidity ratewith open thoracotomy. ROLAND D. PINKHAM (Seattle, Wash.): I do not actually disagree with the authors except in this regard: what we are actually using this procedure for is to make a diagnosis. This can be accomplished either by bronchoscopy or needle biopsy, or perhaps through mediastinoscopy, which is the method we prefer. Certainly, all surgeons who are performing pulmonary operations for carcinoma are discouraged with the results, because these patients are seeking treatment even later than they have done previously; also, I suspect that general practitioners are not discovering these cases as soon as we hoped they would. However, in aspirating these lesions for biopsy, the determination of the accuracy, including both the pathologic interpretation as well as obtaining positive results, is open to a great deal of diverse opinions, depending upon the hospital and the pathologist under discussion. We have aspirated a few peripheral lesions, and I still would advise this procedure in certain instances in which operation is not going to be performed and this technic is being carried out solely for diagnosis. However, we now use mediastinoscopy for diagnosis of the spread of lesions, and find that in random studies on carcinoma of the lung positive evidence of metastasis in the subcarinal and peribronchial nodes was found in 80 per cent of the cases. I believe that this is of greater value to us, for then surgery is not indicated with positive subcarinal node spread, although irradiation, if anything, is considered. Thus, using mediastinoscopy for diagnosis, we have approximately the same positive diagnostic
acumen as is obtained with needle biopsy, and with less morbidity, and definitely more information as to the justification for surgical exploration. ROBERT W. JAMPLIS (closing): When my colleague in the radiology department, Dr. Stevens, returned from a sabbatical in Sweden where he was working with Dr. Morgenstern, he wanted to use needle aspiration much more widely than it was employed at the time. I was skeptical about the procedure at first. However, I have been very gratified with the results and have found it particularly helpful in patients with malignant lesions, for which preoperative irradiation is being used. We have not had any bad experience to date because we follow the technic meticulously and, as in everything else, success is directly proportional to the interest of the physician. Dr. Connolly, I firmly believe the procedure is best carried out by the radiologist since he is more adept at working in the dark with the fluoroscopic screen. If cytologic examination of the lesion does not give us the answer, we proceed directly to aspiration of the lesion, and if we obtain positive results, we proceed with therapy. If the results are still indeterminate, we operate nevertheless, provided the other conventional procedures have not indicated the diagnosis either. Dr. Merdinger, I would caution against the use of a Vim-Silverman needle for localized pulmonary lesions. This type of cutting needle is probably responsible for the massive hemorrhages reported by other authors. However, this type of needle is essential in the diagnosis of diffuse fibrotic diseases. Dr. Pinkham, mediastinoscopy in skilled hands can be a valuable diagnostic and prognostic tool, but cannot be used for lesions which are more peripherally located.