Percutaneous needle aspiration biopsy MICHAEL J. MCLOUGHLIN, MB, B5, MRCP (LOND), FRCR, FRCP[C]; CHIA-SING Ho, MB, B5, FRCP[C]; LIANG-CHE TAO, MD, FRCP[C] This paper reviews the history, technique, applications, advantages, disadvantages and complications of percutaneous needle aspiration biopsy. This technique, particularly when performed with a fine needle (21-gauge or less), is a relatively painless, Inexpensive and safe method of obtaining a pathologic diagnosis, and It can often be carried out at the bedside or in the outpatient department. It complements other methods and may obviate, but never precludes, subsequent excislonal biopsy. Its advantages are Insufficiently recognized. Considerable expertise of the cytopathologist and close cooperation with the clinician are necessary for consistent results.
number of available imaging techniques, the clinician must choose from a variety of methods ranging from exfoliative cytology to excisional biopsy. The risk and discomfort of each method must be balanced against the potential diagnostic yield. In general, a simple safe technique will initially be chosen. Needle aspiration biopsy is a method whereby a very small quantity of tissue, fluid and cells is aspirated from a lesion for cytologic examination. It entails little risk, especially when performed with fine needles (21-gauge or less). Aspiration biopsy must be clearly distinguished from other forms of needle biopsy in Cet article passe en revue l'hlstorlque, which a large needle is used (thus Ia technique, les applications, les increasing the risk of complications) avantages, les d6savantages et les to obtain a core of tissue for hiscomplications de Ia biopsie a l'aiguille tologic examination. par aspiration percutan6e. Cette technique, partlculi.rement lorsqu'.lle Although it had been performed est effectu6e avec une alguille fine intermittently in the second half of (de calibre 21 ou moms), est une the last century and the early years m.thode relativement indolore, peu of this one, diagnostic aspiration coOteuse et sOre d'obtenlr un diagnostic biopsy was first popularized at the pathologique, et souvent elle peut .tre Memorial Hospital for Cancer and r6alls.e au lit du malade ou en Allied Diseases, New York in the clinique externe. Elle compl6mente 1 930s."2 Eighteen-gauge needles were d'autres m6thodes et elle peut 6viter, used, which, in addition to providing sans toutefois 6llmlner, une blopsie. material for cytologic examination, excision subs6quente. Ses avantages might yield fragments of tissue suitne sont pas suffisamment reconnus. able for histologic study. While biopUn nlveau dexpertise consid6rable du cytopathologiste et une 6troite sy with large-bore needles3 became collaberation avec le clinicien sont more popular, European workers n6cessaires pour obtenir des r6sultats continued to develop aspiration biopconcordants. sy using fine needles (21- to 23gauge).4-8 In diagnosing a mass discovered The initial targets were palpable either by clinical examination or by masses, particularly enlarged lymph one or more of the ever-increasing nodes and breast lumps. The development of image intensification and From the departments of radiology and pathology, Toronto General Hospital Readers are referred to the authors' accompanying article beginning on Reprint requests to: Dr. Michael J. page 1311 of this issue of the JourMcLoughlin, Department of radiology, Toronto General Hospital, 101 College naL St., Toronto, Ont. M5G 1L7 1324 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
television facilitated aspiration biopsy of pulmonary lesions under fluoroscopic control."' in the past few years percutaneous fine-needle aspiration of intra-abdominal lesions has become increasingly . In appropriately selected cases aspiration biopsy offers a quick, relatively painless and convenient way of obtaining a pathologic diagnosis. Fine-needle aspiration of a lymph node or of the prostate is easily performed in the outpatient department and may make more elaborate methods of biopsy (excisional or transperineal punch biopsy) unnecessary. Transthoracic and transabdominal biopsy may provide information otherwise obtainable only by thoracotomy or laparotomy. In addition to convenience to the patient and physician, there may be considerable reduction of cost through obviation of other investigations, hospitalization and surgical exploration. Aspiration biopsy has been most useful in patients with suspected malignant disease, and is particularly accurate in the diagnosis of carcinoma. It complements operative and other forms of biopsy, which are indicated when the results of aspiration are inconclusive. Because of its minor nature, aspiration may be used for multiple lesions, may be repeated and is particularly suitable in debilitated patients. On occasion it may be both diagnostic and therapeutic (e.g., in the management of cysts of the breast and kidney). Technique
At present, aspiration is usually performed with fine needles (21- to 23-gauge) of suitable length, except in the lung, where 18- to 20-gauge needles are most commonly used (Table I). Superficial lesions (e.g., enlarged
superficial lymph nodes and breast lumps) are fixed with one hand while the needle, attached to a syringe, is inserted with the other. Continuous suction is applied while the needle is advanced and withdrawn two or three times in different directions. Suction is discontinued and the needle removed. Biopsy takes only a few seconds. Simultaneous manipulation of the needle and application of suction is facilitated by use of the one-handed syringe holder described by Franzen, Giertz and Zajicek' (Fig. 1). Anesthesia is not required for aspiration of superficial lesions, but for deeper lesions the skin and body wall are infiltrated with local anesthetic and a small nick is made with the tip of a scalpel to facilitate entry of the needle. For intrathoracic aspiration the needle and stylet are advanced into the lesion under fluoroscopic control. The stylet is removed and the needle advanced and rotated. Slight negative pressure is applied during withdrawal. Usually a single aspiration is adequate. Transabdominal targets must be localized by palpation or by various radiologic methods, radioisotope studies, ultrasonography or computed tomography. Radiologic methods include intravenous pyelography, angiography, endoscopic retrograde cholangiopancreatography and barium studies. The skin overlying the lesion is marked, and the needle and stylet are inserted through the skin. The stylet is removed and the needle passed into the lesion and rotated; intermittent suction is applied and
released before withdrawal. Several when the cell type may match that aspirations are made in different di- of a known primary tumour or may rections. suggest the primary when this is unPelvic organs, particularly the known. Malignant lymphoma can be prostate, may be aspirated transrec- diagnosed, but excisional biopsy is tally. This is best done with the meth- often necessary for accurate classiod described by Franzen and col- fication. leagues.' The prostate is palpated with the index finger of the left hand, Breast to which is attached a flexible needle Good results in the diagnosis of guide. The syringe holder containing cancer of the breast have been obthe syringe and needle is held in the tained for many years by aspiration right hand. The needle is directed biopsy with medium-sized (18-gauge) into the lesion through the needle needles."' More recently, excellent guide and several aspirations are results have been obtained with fine made. needles at the Radiumhummett in With an air-filled syringe the as- Stockholm" and at other centres.""4'7 pirated material is blown out of the Zajicek and colleagues" reported needle onto slides. Thin smears are a series of 4700 biopsies, of which made and either fixed in alcohol for 1086 were of carcinoma that was Papanicolaou staining or air-dried subsequently histologically proven. for staining by the May-Griinwald- Of the carcinomas 77 % were corGiemsa method. When indicated, rectly diagnosed by aspiration; in material is also prepared for bac- 13 % the biopsy specimens were conteriologic examination. sidered suspicious and in 10% they were falsely negative. There were no Applications false-positive results. At that institution the cytopathologist, in judging Superficial lymph nodes the biopsy specimens to be positive, One of the oldest indications for accepts responsibility for radical masaspiration biopsy is enlarged super- tectomy; operative biopsy is reserved ficial lymph nodes. Early workers for cases in which the biopsy results used medium-sized (1 8-gauge) nee- are suspicious or negative. Others'6"7 dles,"' but many investigators have have found aspiration biopsy helpful confirmed that equally good results in clinical management and advocate may be obtained with fine needles, it for all breast lumps, but confirm which cause minimal discomfort for all diagnoses of cancer with excisionthe patient.8""" Aspiration is most al biopsy. helpful in metastatic carcinoma, Aspiration biopsy is helpful in sev-
FIG. 1-Modification of syringe holder described by Franzen, Giertz and Zajicek,' made at Princess Margaret Hospital, Toronto for Dr. A.R. Harwood, uses disposable syringes and needles. Puncture and suction can be performed with one hand. CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1325
eral circumstances: (a) when the patient has operable cancer and will thus have some time to adjust psychologically to the idea of mastectomy; (b) in confirming that a cancer is inoperable prior to radiotherapy; (c) occasionally when cancer is diagnosed in a lesion that seems clinically benign; and (d) when the lesion is cystic, in which case aspiration may be both diagnostic and therapeutic and is an acceptable method of management provided certain guidelines are strictly followed.28 Lung Percutaneous needle aspiration biopsy of intrathoracic lesions has been practised for many years,""'. and became widely accepted following the development of television fluoroscopy, which allows easy fluoroscopic control of the procedure.9'10'30-32 It is particularly useful in assessing discrete pulmonary lesions greater than 0.5 cm in diameter, for which an accurate diagnosis is obtained in more than 80% of patients. The diagnostic yield from aspiration biopsy is greater than that from any other method except thoracotomy.3"3' In many centres including ours where small-cell (oat-cell) carcinoma is no longer treated surgically, patients may be spared unnecessary thoracotomy by aspiration biopsy. Needles of intermediate size (18to 20-gauge) are usually used, but a recent report suggests that the use of 23-gauge needles can reduce the frequency of complications without reducing accuracy.33 Prostate Aspiration biopsy of the prostate was originally performed transperineally with 1 X-gauge needles,"2'34 but the transrectal fine-needle technique of Franzen and colleagues3 is now preferred. It is safe and accurate, causes little discomfort and can be performed as an outpatient procedure.8 Some have found it as reliable in the diagnosis of carcinoma as transperineal punch biopsy with Silverman and Veenema instruments." Others have found it somewhat less accurate, but prefer it as the initial procedure because of its convenience." If the results of fineneedle biopsy are positive, as they are in approximately 80% of patients with prostatic carcinoma, punch biopsy is unnecessary. 1326
Pancreas Percutaneous fine-needle aspiration has recently been recognized as a reliable, safe method for diagnosing malignant lesions of the pancreas and surrounding structures 14,16,17,10,20 The lesion must be localized prior to biopsy by radiologic methods,'6'7'9"0 ultrasonography'4 or computed tomography. The biopsy specimens are positive in approximately 80% of cases of malignant disease, an accuracy comparable to that of operative biopsy.'0 Some reserve percutaneous biopsy for patients not requiring an operation,'7 but we also recommend preoperative percutaneous biopsy for those who do require an operation because of the potential risk and relatively high frequency (10% to 20%) of falsenegative results of operative biopsy.'0 Liver A few investigators""' have used fine-needle aspiration biopsy to diagnose primary and secondary malignant disease in the liver. Aspiration biopsy not fluoroscopically guided gave positive results in 77% of patients with malignant disease in one series," and ultrasonically guided fine-needle aspiration was superior to punch biopsy with the Menghini needle in another." Accuracy may be increased by directing the needle into a lesion localized by radioisotope scanning, ultrasonography or other means, or by moving the needle in several directions so as to sample a large volume of liver in both lobes. We believe that the increased accuracy and the very low risk make fine-needle biopsy the preferred procedure for the patient with suspected malignant disease. Conventional punch biopsy remains the procedure of choice in patients with non-neoplastic liver disease. Kidney Renal masses are commonly detected by intravenous pyelography, and most are either benign cysts or renal cell carcinomas. Ultrasonography is a useful second step that will usually differentiate solid from cystic lesions. Angiography is diagnostic for most carcinomas, and cyst puncture may be performed to confirm a diagnosis of simple cyst.
CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
Fine-needle aspiration biopsy of renal masses is infrequently performed, but is diagnostic in 71% to 88% of tumours.'0""38 Some have recommended needling all renal masses following intravenous pyelography and ultrasonography, either for cyst puncture or for aspiration biopsy." We believe that aspiration biopsy is underused and is certainly indicated in cases of renal masses for which the results of ultrasonography and angiography are inconclusive. As in the liver, conventional punch biopsy of the kidney is necessary for the diagnosis of parenchymal disease. Spleen Aspiration biopsy of the spleen has been recognized for many years as a method for assisting in the diagnosis of a variety of hematologic diseases.4'7'37'38 It has not been used as widely as it deserves because of an unfounded fear of the risks involved and of presumed difficulties in interpretation . Splenic aspiration is essentially a hematologic technique, analogous to bone marrow aspiration and examination of a blood film. It is strongly indicated in the patient with splenomegaly in whom examination of the blood and bone marrow has been unhelpful. It may provide useful diagnostic information in a variety of disorders, including osteosclerotic anemia, extramedullary hematopoiesis, Gaucher's disease and amyThyroid A number of investigators have found fine-needle aspiration biopsy of value in various thyroid disorders.8'40-43 It is highly accurate in confirming a diagnosis of Hashimoto's disease or lymphocytic thyroiditis.40'4' Although biopsy will de8,40 be tect most carcinomas, many lieve that it is redundant since suspicious nodules usually require surgery.43 Biopsy is valuable in confirming the presence of metastases from thyroid carcinoma in cervical lymph nodes. Salivary glands Considerable work has been done on fine-needle aspiration biopsy of the salivary glands by Scandinavian workers,8'44'.' but the method is not widely popular because of difficulties in interpretation arising from the va-
riety of tumour types and the heterogenous cell populations of individual tumours.44'.' In all cases lumps suspected of being neoplastic require excisional biopsy, the aim being complete removal of benign lesions and "marginal security" with those subsequently shown to be malignant. Bone Bone marrow aspiration is the most widely accepted form of aspiration biopsy. Biopsy of focal bone lesions, particularly neoplasms, may be performed with needles of large,46 medium'0 or fine calibre.8'47 The examination is best performed under fluoroscopic control. Fine-needle aspiration is simple and relatively painless, and the accuracy is comparable to that of biopsy with larger needles.47 If the attempt at fine-needle aspiration fails because the bony cortex of the lesion cannot be penetrated, a needle of larger calibre may be tried.8 Fine-needle aspiration biopsy is particularly useful in the diagnosis of metastatic carcinoma and multiple myeloma.8'47 Other regions Any intra-abdominal or retroperitoneal mass can be aspirated with a fine needle.'7'18 Retroperitoneal lymphoma may also be diagnosed in this way, but, as with superficial lymph nodes, classification may prove difficult. Aspiration biopsy of lesions of the maxillary antrum, upper and lower jaws, tongue, tonsil and nasopharynx has also been performed with needles of medium"2 and, more recently, fine calibre.48'49 Operative biopsy Biopsy performed at the time of an operation is usually incisional, but aspiration biopsy had advantages in some instances. In a recent review of the literature on operative pancreatic biopsy'0 we found a low frequency of complications attributed to incisional (wedge) and needle (punch) biopsy, but no complications from operative fineneedle aspiration biopsy. Since aspiration biopsy had a high yield in the diagnosis of pancreatic carcinoma, it appears to be the most appropriate method of studying the pancreas at the time of operation. In some areas (e.g., the nasopharynx) that are difficult to ex-
amine, and where excisional biopsy of malignant tumours not infrequentiy yields negative results, fine-needle aspiration may be performed at the same time as incisional biopsy to increase the diagnostic yield.49 Disadvantages and complications The major disadvantage of needle aspiration is the small amount of material available for examination; this calls for considerable expertise of the cytopathologist. Close cooperation between the clinician and the cytopathologist and some experience in biopsy technique are required for consistent results. Superficial lesions are best aspirated by either the cytopathologist or a clinician with a special interest in providing continuing patient care. Deep lesions should be aspirated by the appropriate specialist - the thoracic surgeon or urologist, or an experienced radiologist. Complications of aspiration biopsy depend on the site of biopsy and the size of the needle. With superficial lesions they are minimal and limited to an occasional small hematoma. Minor complications of transrectal fine-needle aspiration biopsy of the prostate include epididymitis, transient hematuria, hemospermia and febrile reactions; they occur in less than 1 % of patients.8'50 Th. only serious complications reported in a series of 14 000 biopsies were four cases of coliform septicemia, one of which was fatal; this rate of complications was considerably less than that observed with transperineal punch . Although both solid and hollow viscera may be transfixed during percutaneous fine-needle aspiration biopsy of intra-abdominal organs, the rate of complications is low. Stormby and Akerman'1 found no complications in more than 1000 liver aspirations, and Lundquist12 noted one complication (intrahepatic hematoma) in 2611 liver aspirations. S6derstrom38 found no complications in more than 1000 splenic punctures. Only one complication (exacerbation of pancreatitis) was detected in a review of pancreatic aspirations in 99 patients.20 There are also single case reports of biliary peritonitis52 and intraperitoneal hemorrhage53 following liver aspiration; the latter is the only fatal case we are aware of, and it occurred in a patient with
hepatoma, cirrhosis and liver failure. Complications occur most commonly with intrathoracic biopsy. They include pneumothorax, intrathoracic hemorrhage and hemoptysis. In a recent review of 1562 aspiration biopsies based on the results of a questionnaire,H the rates of pneumothorax requiring treatment and of major hemorrhage were 7.0% and 0.2% respectively, and the mortality was 0.1 %. It has been suggested that the use of 23-gauge needles may reduce the frequency of these complications.33 In any form of needle biopsy, possible seeding of the needle track with malignant cells must be considered. In a recent review we found that this almost invariably followed punch biopsy with large-bore needles, most commonly transperineal biopsy of the prostate with a Silverman needle.20 We found only one documented case of tumour recurrence attributed to aspiration biopsy with a mediumsized needle.. No evidence of tumour spread was found following 626 aspiration biopsies of the lung19 or in 459 patients with carcinoma of the prostate,56 641 with metastatic carcinoma in cervical lymph nodes12 and 147 with pleomorphic adenomas of the salivary glands.56 The possibility of widespread dissemination of tumour cells by biopsy must also be considered, but studies of osteogenic sarcoma57 and of breast,58 kidney59 and lung cancer55 have failed to show evidence of reduced survival in patients who undergo aspiration biopsy. References 1. STEWART FW: The diagnosis of tumors by aspiration. Am J Pathol 9 (suppl): 801, 1933 2. MARTIN HE, ELLIS ER: Aspiration biopsy. Surg Gynecol Obstet 59: 578, 1934 3. SILVERM.AN I: A new biopsy needle.
Am J Surg 40: 671, 1938 4. LOPES CARDOZO P: Clinical Cytology Using the May-Grunwald-Giemsa Stained Smear, vol 1, Stafleu, Leyden, 1954 5. FRANZEN 5, GIERTZ G, ZAJICEK J: Cytological diagnosis of prostatic tumour by transrectal aspiration biopsy: a preliminary report. Br I Urol
32: 193, 1960 6. BERG 1W: The aspiration biopsy smear, in Diagnostic Cytology and its Histopathologic Bases, vol 1, Koss LG, DURFEE GR (eds), Lippincott, Philadelphia, 1961, p 311 7. SODERSTROM N: Fine-Needle Aspira-
CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1327
tion Biopsy, Grune, New York, 1966 8. Espos'ri P-L, FRANZEN 5, ZAJICEK J: The aspiration biopsy smear, in Diagnostic Cytology and its Histopathologic Bases, vol 2, Koss LG, DURFEE GR (eds), Lippincott, Philadelphia, 1968, p 565 9. DAHLGREN 5, NORDENSTROM B: Transthoracic Needle Biopsy, Year Bk Med, Chicago, 1966 10. LALLI AF: The direct fluoroscopically guided approach to renal, thoracic and skeletal lesions. Curr Probi' Radiol 2: 1, 1972 11. HENDRY WE, WILLIAMS JP: Transrectal prostatic biopsy. Br Med J 4: 595, 1971 12. LuNDQUIsT A: Fine-needle aspiration biopsy of the liver. Applications in clinical diagnosis and investigation.
Acta Med Scand (Suppl]: no 520, 1971 13. OSCARSON J, STORMBY N, SUNDOREN R: Selective angiography in fineneedle aspiration cytodiagnosis of gastric and pancreatic tumors. A cia Ra-
diol [Diagn] (Stockh) 12: 737, 1972 14. HANCKE 5, HOLM HH, KocH F: Ultrasonically guided percutaneous fine needle biopsy of the pancreas. Surg
Gynecol Obstet 140: 361, 1975 15. HOLM HH, PEDERSEN JF, KRISTENSEN JK, et al: Ultrasonically guided percutaneous puncture. Radiol Clin North Am 13: 493, 1975 16. TYLEN U, ARNESJO B, LINDBERG LG, et al: Percutaneous biopsy of carcinoma of the pancreas guided by angio-
graphy. Surg Gynecol Obstet 142: 737, 1976 17. GOLDSTEIN HM, ZORNOZA J, WALLACE 5, et al: Percutaneous fine needle aspiration biopsy of pancreatic and other abdominal masses. Radiology 123: 319, 1977 18. ZORNOZA J, JoNsso. K, WALLACE S, et al: Fine needle aspiration biopsy of retroperitoneal lymph nodes and abdominal masses: an updated report.
Radiology 125: 87, 1977 19. Ho C-S, MCLOUGHLIN MJ, MCHATTIE JD, et al: Percutaneous fine needle aspiration biopsy of pancreas following endoscopic retrograde cholangiopancreatography. Ibid, p 351 20. MCLOUGHLIN MJ, Ho C-S, LANGER B, et al: Fine needle aspiration biopsy of malignant lesions in and around the pancreas. Cancer 41: 2413, 1978 21. SMITH IH, FISHER JH, Lorr JS, et al: The cytological diagnosis of solid tumours by small needle aspiration and its influence on cancer clinic practice.
Can Med Assoc J 80: 855, 1959 22. ENGZELL U, JAKOBSSON PA, SIGIJRD-
24. STAVRIC GD, TEVCEV DT, KAFTAND-
JIEV DR, et al: Aspiration biopsy cytologic method in diagnosis of breast lesions: a critical review of 250 cases. Acta Cytol (Baltimore) 17: 188, 1973 25. KLINE TS, NEAL HS: Needle aspiration of the breast - why bother? Acta Cytol (Baltimore) 20: 324, 1976 26. ZAJDELA L, GHossEIN NA, PILLERON
JP, et al: The value of aspiration cytology in the diagnosis of breast cancer: experience at the Fondation Curie. Cancer 35: 499, 1975 27. FURNIVAL CM, HUGHES HE, HOCKING MA, et al: Aspiration cytology in breast cancer. Its relevance to diagnosis. Lancet 2: 446, 1975 28. ABRAHAMSON DJ: A clinical evaluation of aspiration of cysts of the breast. Surg Gynecol Obstet 139: 531, 1974 29. LAUBY VW, BURNETr WE, ROSEMOND GP, et al: Value and risk of biopsy of pulmonary lesions by needle aspiration. Twenty-one years' experience.
J Thorac Cardiovasc Surg 49: 159, 1965 30. STEVENS GM, WEIGEN iF, LILLINCTON GA: Needle aspiration biopsy of localized pulmonary lesions with amplified fluoroscopic guidance. Am J Roentgenol Radium Ther Nuci Med 103: 561, 1968 31. SANDERS DE, THOMPSON DW, PUDDEN BJE: Percutaneous aspiration lung
biopsy. Can Med Assoc J 104: 139, 1971 32. SARGENT EN, TURNER AF, GORDONSON J, et al: Percutaneous pulmonary needle biopsy: report of 350 patients. Am J Roentgenol Radium Tlaer Nuci Med 122: 758, 1974 33. ZORNOZA J, SNOW J JR, LUKEMAN JM.
et al: Aspiration biopsy of discrete pulmonary lesions using a thin needle. Results in the first 100 cases. Radiology 123: 519, 1977 34. FERGUSON RS: Diagnosis and treatment of early carcinoma of the prostate. J Urol 37: 774, 1937 35. ANDERSSON K, JONSSON G, BRUNK U: Puncture biopsy of the prostate in the diagnosis of prostatic cancer. Scand
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of
cytophotometry.
sies. Acta Cytol (Baltimore) 11: 470, 1967 46. SCHAJOWICZ F, DERQUI JC: Puncture biopsy in lesions of the locomotor system: review of result in 4050 cases, including 941 vertebral punctures. Cancer 21: 531, 1968 47. AKERMAN
M,
BERG
NO,
PERssoN
BM: Fine needle aspiration biopsy in the evaluation of tumor-like lesions of
bone. Acta Orthop Scand 47: 129, 1976 48. THOMSEN J, ANDREASSEN JC, BANGSBO C: Fine-needle aspiration biopsy of tumors of the head and neck. I
Laryngol Otol 87: 1211, 1973 49. SAMUEL PR: Aspiration biopsy. An aid in the diagnosis of para-nasal tu-
mours. I Laryngol Otol 90: 253, 1976 50. Es.osri P-L, EL MAN A, NORLEN H: Complications of transrectal biopsy of the prostate. Scand I Urol Nephrol 9: 208, 1975 51. STORMBY N, AKERMAN M: Aspiration
cytology in the diagnosis of granulomatous liver lesions. Acta Cytol (Baltimore) 17: 200, 1973 52. SCHULZ TB: Fine-needle aspiration biopsy of the liver complicated with bile peritonitis. A cta Med Scand 199: 141, 1976
53. RIsi.. H, FRIMAN C: Fatality after fine-needle aspiration biopsy of liver (C). Br Med 1 1: 517, 1975 54. HERMAN PG, HESSEL SJ: The diag11, 1977 55. SINNER WN, ZAJICEK J: Implantation
37. MORRISON M, SAMWICK AA, RuBIN-
STEIN J, et al: Splenic aspiration. Clin. ical and hematologic considerations based on observation in 105 cases. JAMA 146: 1575, 1951 38. SODERSTROM N: How to use cytodiagnostic spleen puncture. Acta Med
40. EINHORN J, FRANZEN S: Thin-needle
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45. ENEROTH C-M, FRANZEN 5, ZAJICEK J, et al: Aspiration of salivary gland tumors. A critical review of 910 biop-
taneous cytological aspiration biopsy in the diagnosis of renal tumours. A niz Chir Gynaecol Fenn 58: 304, 1969
23. ZAJICEK J, CASPERSSON T, JAKOBSSON
diagnostic
L, et al: Fine needle and open biopsy in thyroid disorders. Acta C/dr Scand 141: 20, 1975 44. MAVEC P, ENEROTH C-M, FRANZEN 5, et al: Aspiration bio.psy of salivary gland tumours. 1. Correlation of cytologic reports from 652 aspiration biopsies with clinical and histologic findings. Acta Otolaryngol (Stock/i) 58: 471, 1964
nostic accuracy and complications of closed lung biopsies. Radiology 125:
39. PASTERNACK A: Fine-needle aspiration biopsy of the spleen in diagnosis of generalized amyloidosis. Br Med J 2: 20, 1974
Ada Cytol (Baltimore) 14: 370, 1970
43. KOLENDORF K, HANSEN JB, ENGBERG
36. ALFTHAN 0, KOIVUNIEMI A: Percu-
SON A, et al: Aspiration biopsy of metastatic carcinoma in lymph nodes of the neck. A review of 1101 consecutive cases. A cia Otolaryngol (Stockh) 72: 138, 1971 P, et al: Cytologic diagnosis of mammary tumors from aspiration biopsy smears. Comparison of cytologic and histologic findings in 2,111 lesions and
Ct al: Application of special diagnostic techniques in the management of nodular goitre. Can Med Assoc 1 115: 35, 1976
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biopsy in the diagnosis of thyroid disease. Acta Radiol 58: 321, 1962 41. CROCKFORD PM, BAIN GO: Fineneedle aspiration biopsy of the thyroid. Can Med Assoc J 110: 1029, 1974 42. WALFISH PG, MISKIN M, ROSEN IB,
1328 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
metastasis after percutaneous transthoracic needle aspiration biopsy. Acta
Radiol [Diagn] (Stock/i) 17: 473, 1976 56. ENGZELL U, Esiosri P-L, Runio C,
et al: Investigation on tumour spread in connection with aspiration biopsy. Acta Radiol [Ther] (Stock/i) 10: 385, 1971 57. SNYDER RE, COLEY BL: Further studies on the diagnosis of bone tumors by aspiration biopsy. Surg Gynecol Obstet 80: 517, 1945 58. BERG JW, ROBBINS GF: A late look at the safety of aspiration biopsy. Cancer 15: 826, 1962 59. VON SCHREEB T, ARNER 0, SKOvSTED G: Renal adenocarcinoma. Is there a risk of spreading tumour cells in diagnostic puncture? Scand I Urol Nephrol
1: 270, 1976
number of available imaging techniques, the clinician must choose from a variety of methods ranging from exfoliative cytology to excisional biopsy. The risk and discomfort of each method must be balanced against the potential diagnostic yield. In general, a simple safe technique will initially be chosen. Needle aspiration biopsy is a method whereby a very small quantity of tissue, fluid and cells is aspirated from a lesion for cytologic examination. It entails little risk, especially when performed with fine needles (21-gauge or less). Aspiration biopsy must be clearly distinguished from other forms of needle biopsy in Cet article passe en revue l'hlstorlque, which a large needle is used (thus Ia technique, les applications, les increasing the risk of complications) avantages, les d6savantages et les to obtain a core of tissue for hiscomplications de Ia biopsie a l'aiguille tologic examination. par aspiration percutan6e. Cette technique, partlculi.rement lorsqu'.lle Although it had been performed est effectu6e avec une alguille fine intermittently in the second half of (de calibre 21 ou moms), est une the last century and the early years m.thode relativement indolore, peu of this one, diagnostic aspiration coOteuse et sOre d'obtenlr un diagnostic biopsy was first popularized at the pathologique, et souvent elle peut .tre Memorial Hospital for Cancer and r6alls.e au lit du malade ou en Allied Diseases, New York in the clinique externe. Elle compl6mente 1 930s."2 Eighteen-gauge needles were d'autres m6thodes et elle peut 6viter, used, which, in addition to providing sans toutefois 6llmlner, une blopsie. material for cytologic examination, excision subs6quente. Ses avantages might yield fragments of tissue suitne sont pas suffisamment reconnus. able for histologic study. While biopUn nlveau dexpertise consid6rable du cytopathologiste et une 6troite sy with large-bore needles3 became collaberation avec le clinicien sont more popular, European workers n6cessaires pour obtenir des r6sultats continued to develop aspiration biopconcordants. sy using fine needles (21- to 23gauge).4-8 In diagnosing a mass discovered The initial targets were palpable either by clinical examination or by masses, particularly enlarged lymph one or more of the ever-increasing nodes and breast lumps. The development of image intensification and From the departments of radiology and pathology, Toronto General Hospital Readers are referred to the authors' accompanying article beginning on Reprint requests to: Dr. Michael J. page 1311 of this issue of the JourMcLoughlin, Department of radiology, Toronto General Hospital, 101 College naL St., Toronto, Ont. M5G 1L7 1324 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
television facilitated aspiration biopsy of pulmonary lesions under fluoroscopic control."' in the past few years percutaneous fine-needle aspiration of intra-abdominal lesions has become increasingly . In appropriately selected cases aspiration biopsy offers a quick, relatively painless and convenient way of obtaining a pathologic diagnosis. Fine-needle aspiration of a lymph node or of the prostate is easily performed in the outpatient department and may make more elaborate methods of biopsy (excisional or transperineal punch biopsy) unnecessary. Transthoracic and transabdominal biopsy may provide information otherwise obtainable only by thoracotomy or laparotomy. In addition to convenience to the patient and physician, there may be considerable reduction of cost through obviation of other investigations, hospitalization and surgical exploration. Aspiration biopsy has been most useful in patients with suspected malignant disease, and is particularly accurate in the diagnosis of carcinoma. It complements operative and other forms of biopsy, which are indicated when the results of aspiration are inconclusive. Because of its minor nature, aspiration may be used for multiple lesions, may be repeated and is particularly suitable in debilitated patients. On occasion it may be both diagnostic and therapeutic (e.g., in the management of cysts of the breast and kidney). Technique
At present, aspiration is usually performed with fine needles (21- to 23-gauge) of suitable length, except in the lung, where 18- to 20-gauge needles are most commonly used (Table I). Superficial lesions (e.g., enlarged
superficial lymph nodes and breast lumps) are fixed with one hand while the needle, attached to a syringe, is inserted with the other. Continuous suction is applied while the needle is advanced and withdrawn two or three times in different directions. Suction is discontinued and the needle removed. Biopsy takes only a few seconds. Simultaneous manipulation of the needle and application of suction is facilitated by use of the one-handed syringe holder described by Franzen, Giertz and Zajicek' (Fig. 1). Anesthesia is not required for aspiration of superficial lesions, but for deeper lesions the skin and body wall are infiltrated with local anesthetic and a small nick is made with the tip of a scalpel to facilitate entry of the needle. For intrathoracic aspiration the needle and stylet are advanced into the lesion under fluoroscopic control. The stylet is removed and the needle advanced and rotated. Slight negative pressure is applied during withdrawal. Usually a single aspiration is adequate. Transabdominal targets must be localized by palpation or by various radiologic methods, radioisotope studies, ultrasonography or computed tomography. Radiologic methods include intravenous pyelography, angiography, endoscopic retrograde cholangiopancreatography and barium studies. The skin overlying the lesion is marked, and the needle and stylet are inserted through the skin. The stylet is removed and the needle passed into the lesion and rotated; intermittent suction is applied and
released before withdrawal. Several when the cell type may match that aspirations are made in different di- of a known primary tumour or may rections. suggest the primary when this is unPelvic organs, particularly the known. Malignant lymphoma can be prostate, may be aspirated transrec- diagnosed, but excisional biopsy is tally. This is best done with the meth- often necessary for accurate classiod described by Franzen and col- fication. leagues.' The prostate is palpated with the index finger of the left hand, Breast to which is attached a flexible needle Good results in the diagnosis of guide. The syringe holder containing cancer of the breast have been obthe syringe and needle is held in the tained for many years by aspiration right hand. The needle is directed biopsy with medium-sized (18-gauge) into the lesion through the needle needles."' More recently, excellent guide and several aspirations are results have been obtained with fine made. needles at the Radiumhummett in With an air-filled syringe the as- Stockholm" and at other centres.""4'7 pirated material is blown out of the Zajicek and colleagues" reported needle onto slides. Thin smears are a series of 4700 biopsies, of which made and either fixed in alcohol for 1086 were of carcinoma that was Papanicolaou staining or air-dried subsequently histologically proven. for staining by the May-Griinwald- Of the carcinomas 77 % were corGiemsa method. When indicated, rectly diagnosed by aspiration; in material is also prepared for bac- 13 % the biopsy specimens were conteriologic examination. sidered suspicious and in 10% they were falsely negative. There were no Applications false-positive results. At that institution the cytopathologist, in judging Superficial lymph nodes the biopsy specimens to be positive, One of the oldest indications for accepts responsibility for radical masaspiration biopsy is enlarged super- tectomy; operative biopsy is reserved ficial lymph nodes. Early workers for cases in which the biopsy results used medium-sized (1 8-gauge) nee- are suspicious or negative. Others'6"7 dles,"' but many investigators have have found aspiration biopsy helpful confirmed that equally good results in clinical management and advocate may be obtained with fine needles, it for all breast lumps, but confirm which cause minimal discomfort for all diagnoses of cancer with excisionthe patient.8""" Aspiration is most al biopsy. helpful in metastatic carcinoma, Aspiration biopsy is helpful in sev-
FIG. 1-Modification of syringe holder described by Franzen, Giertz and Zajicek,' made at Princess Margaret Hospital, Toronto for Dr. A.R. Harwood, uses disposable syringes and needles. Puncture and suction can be performed with one hand. CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1325
eral circumstances: (a) when the patient has operable cancer and will thus have some time to adjust psychologically to the idea of mastectomy; (b) in confirming that a cancer is inoperable prior to radiotherapy; (c) occasionally when cancer is diagnosed in a lesion that seems clinically benign; and (d) when the lesion is cystic, in which case aspiration may be both diagnostic and therapeutic and is an acceptable method of management provided certain guidelines are strictly followed.28 Lung Percutaneous needle aspiration biopsy of intrathoracic lesions has been practised for many years,""'. and became widely accepted following the development of television fluoroscopy, which allows easy fluoroscopic control of the procedure.9'10'30-32 It is particularly useful in assessing discrete pulmonary lesions greater than 0.5 cm in diameter, for which an accurate diagnosis is obtained in more than 80% of patients. The diagnostic yield from aspiration biopsy is greater than that from any other method except thoracotomy.3"3' In many centres including ours where small-cell (oat-cell) carcinoma is no longer treated surgically, patients may be spared unnecessary thoracotomy by aspiration biopsy. Needles of intermediate size (18to 20-gauge) are usually used, but a recent report suggests that the use of 23-gauge needles can reduce the frequency of complications without reducing accuracy.33 Prostate Aspiration biopsy of the prostate was originally performed transperineally with 1 X-gauge needles,"2'34 but the transrectal fine-needle technique of Franzen and colleagues3 is now preferred. It is safe and accurate, causes little discomfort and can be performed as an outpatient procedure.8 Some have found it as reliable in the diagnosis of carcinoma as transperineal punch biopsy with Silverman and Veenema instruments." Others have found it somewhat less accurate, but prefer it as the initial procedure because of its convenience." If the results of fineneedle biopsy are positive, as they are in approximately 80% of patients with prostatic carcinoma, punch biopsy is unnecessary. 1326
Pancreas Percutaneous fine-needle aspiration has recently been recognized as a reliable, safe method for diagnosing malignant lesions of the pancreas and surrounding structures 14,16,17,10,20 The lesion must be localized prior to biopsy by radiologic methods,'6'7'9"0 ultrasonography'4 or computed tomography. The biopsy specimens are positive in approximately 80% of cases of malignant disease, an accuracy comparable to that of operative biopsy.'0 Some reserve percutaneous biopsy for patients not requiring an operation,'7 but we also recommend preoperative percutaneous biopsy for those who do require an operation because of the potential risk and relatively high frequency (10% to 20%) of falsenegative results of operative biopsy.'0 Liver A few investigators""' have used fine-needle aspiration biopsy to diagnose primary and secondary malignant disease in the liver. Aspiration biopsy not fluoroscopically guided gave positive results in 77% of patients with malignant disease in one series," and ultrasonically guided fine-needle aspiration was superior to punch biopsy with the Menghini needle in another." Accuracy may be increased by directing the needle into a lesion localized by radioisotope scanning, ultrasonography or other means, or by moving the needle in several directions so as to sample a large volume of liver in both lobes. We believe that the increased accuracy and the very low risk make fine-needle biopsy the preferred procedure for the patient with suspected malignant disease. Conventional punch biopsy remains the procedure of choice in patients with non-neoplastic liver disease. Kidney Renal masses are commonly detected by intravenous pyelography, and most are either benign cysts or renal cell carcinomas. Ultrasonography is a useful second step that will usually differentiate solid from cystic lesions. Angiography is diagnostic for most carcinomas, and cyst puncture may be performed to confirm a diagnosis of simple cyst.
CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
Fine-needle aspiration biopsy of renal masses is infrequently performed, but is diagnostic in 71% to 88% of tumours.'0""38 Some have recommended needling all renal masses following intravenous pyelography and ultrasonography, either for cyst puncture or for aspiration biopsy." We believe that aspiration biopsy is underused and is certainly indicated in cases of renal masses for which the results of ultrasonography and angiography are inconclusive. As in the liver, conventional punch biopsy of the kidney is necessary for the diagnosis of parenchymal disease. Spleen Aspiration biopsy of the spleen has been recognized for many years as a method for assisting in the diagnosis of a variety of hematologic diseases.4'7'37'38 It has not been used as widely as it deserves because of an unfounded fear of the risks involved and of presumed difficulties in interpretation . Splenic aspiration is essentially a hematologic technique, analogous to bone marrow aspiration and examination of a blood film. It is strongly indicated in the patient with splenomegaly in whom examination of the blood and bone marrow has been unhelpful. It may provide useful diagnostic information in a variety of disorders, including osteosclerotic anemia, extramedullary hematopoiesis, Gaucher's disease and amyThyroid A number of investigators have found fine-needle aspiration biopsy of value in various thyroid disorders.8'40-43 It is highly accurate in confirming a diagnosis of Hashimoto's disease or lymphocytic thyroiditis.40'4' Although biopsy will de8,40 be tect most carcinomas, many lieve that it is redundant since suspicious nodules usually require surgery.43 Biopsy is valuable in confirming the presence of metastases from thyroid carcinoma in cervical lymph nodes. Salivary glands Considerable work has been done on fine-needle aspiration biopsy of the salivary glands by Scandinavian workers,8'44'.' but the method is not widely popular because of difficulties in interpretation arising from the va-
riety of tumour types and the heterogenous cell populations of individual tumours.44'.' In all cases lumps suspected of being neoplastic require excisional biopsy, the aim being complete removal of benign lesions and "marginal security" with those subsequently shown to be malignant. Bone Bone marrow aspiration is the most widely accepted form of aspiration biopsy. Biopsy of focal bone lesions, particularly neoplasms, may be performed with needles of large,46 medium'0 or fine calibre.8'47 The examination is best performed under fluoroscopic control. Fine-needle aspiration is simple and relatively painless, and the accuracy is comparable to that of biopsy with larger needles.47 If the attempt at fine-needle aspiration fails because the bony cortex of the lesion cannot be penetrated, a needle of larger calibre may be tried.8 Fine-needle aspiration biopsy is particularly useful in the diagnosis of metastatic carcinoma and multiple myeloma.8'47 Other regions Any intra-abdominal or retroperitoneal mass can be aspirated with a fine needle.'7'18 Retroperitoneal lymphoma may also be diagnosed in this way, but, as with superficial lymph nodes, classification may prove difficult. Aspiration biopsy of lesions of the maxillary antrum, upper and lower jaws, tongue, tonsil and nasopharynx has also been performed with needles of medium"2 and, more recently, fine calibre.48'49 Operative biopsy Biopsy performed at the time of an operation is usually incisional, but aspiration biopsy had advantages in some instances. In a recent review of the literature on operative pancreatic biopsy'0 we found a low frequency of complications attributed to incisional (wedge) and needle (punch) biopsy, but no complications from operative fineneedle aspiration biopsy. Since aspiration biopsy had a high yield in the diagnosis of pancreatic carcinoma, it appears to be the most appropriate method of studying the pancreas at the time of operation. In some areas (e.g., the nasopharynx) that are difficult to ex-
amine, and where excisional biopsy of malignant tumours not infrequentiy yields negative results, fine-needle aspiration may be performed at the same time as incisional biopsy to increase the diagnostic yield.49 Disadvantages and complications The major disadvantage of needle aspiration is the small amount of material available for examination; this calls for considerable expertise of the cytopathologist. Close cooperation between the clinician and the cytopathologist and some experience in biopsy technique are required for consistent results. Superficial lesions are best aspirated by either the cytopathologist or a clinician with a special interest in providing continuing patient care. Deep lesions should be aspirated by the appropriate specialist - the thoracic surgeon or urologist, or an experienced radiologist. Complications of aspiration biopsy depend on the site of biopsy and the size of the needle. With superficial lesions they are minimal and limited to an occasional small hematoma. Minor complications of transrectal fine-needle aspiration biopsy of the prostate include epididymitis, transient hematuria, hemospermia and febrile reactions; they occur in less than 1 % of patients.8'50 Th. only serious complications reported in a series of 14 000 biopsies were four cases of coliform septicemia, one of which was fatal; this rate of complications was considerably less than that observed with transperineal punch . Although both solid and hollow viscera may be transfixed during percutaneous fine-needle aspiration biopsy of intra-abdominal organs, the rate of complications is low. Stormby and Akerman'1 found no complications in more than 1000 liver aspirations, and Lundquist12 noted one complication (intrahepatic hematoma) in 2611 liver aspirations. S6derstrom38 found no complications in more than 1000 splenic punctures. Only one complication (exacerbation of pancreatitis) was detected in a review of pancreatic aspirations in 99 patients.20 There are also single case reports of biliary peritonitis52 and intraperitoneal hemorrhage53 following liver aspiration; the latter is the only fatal case we are aware of, and it occurred in a patient with
hepatoma, cirrhosis and liver failure. Complications occur most commonly with intrathoracic biopsy. They include pneumothorax, intrathoracic hemorrhage and hemoptysis. In a recent review of 1562 aspiration biopsies based on the results of a questionnaire,H the rates of pneumothorax requiring treatment and of major hemorrhage were 7.0% and 0.2% respectively, and the mortality was 0.1 %. It has been suggested that the use of 23-gauge needles may reduce the frequency of these complications.33 In any form of needle biopsy, possible seeding of the needle track with malignant cells must be considered. In a recent review we found that this almost invariably followed punch biopsy with large-bore needles, most commonly transperineal biopsy of the prostate with a Silverman needle.20 We found only one documented case of tumour recurrence attributed to aspiration biopsy with a mediumsized needle.. No evidence of tumour spread was found following 626 aspiration biopsies of the lung19 or in 459 patients with carcinoma of the prostate,56 641 with metastatic carcinoma in cervical lymph nodes12 and 147 with pleomorphic adenomas of the salivary glands.56 The possibility of widespread dissemination of tumour cells by biopsy must also be considered, but studies of osteogenic sarcoma57 and of breast,58 kidney59 and lung cancer55 have failed to show evidence of reduced survival in patients who undergo aspiration biopsy. References 1. STEWART FW: The diagnosis of tumors by aspiration. Am J Pathol 9 (suppl): 801, 1933 2. MARTIN HE, ELLIS ER: Aspiration biopsy. Surg Gynecol Obstet 59: 578, 1934 3. SILVERM.AN I: A new biopsy needle.
Am J Surg 40: 671, 1938 4. LOPES CARDOZO P: Clinical Cytology Using the May-Grunwald-Giemsa Stained Smear, vol 1, Stafleu, Leyden, 1954 5. FRANZEN 5, GIERTZ G, ZAJICEK J: Cytological diagnosis of prostatic tumour by transrectal aspiration biopsy: a preliminary report. Br I Urol
32: 193, 1960 6. BERG 1W: The aspiration biopsy smear, in Diagnostic Cytology and its Histopathologic Bases, vol 1, Koss LG, DURFEE GR (eds), Lippincott, Philadelphia, 1961, p 311 7. SODERSTROM N: Fine-Needle Aspira-
CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1327
tion Biopsy, Grune, New York, 1966 8. Espos'ri P-L, FRANZEN 5, ZAJICEK J: The aspiration biopsy smear, in Diagnostic Cytology and its Histopathologic Bases, vol 2, Koss LG, DURFEE GR (eds), Lippincott, Philadelphia, 1968, p 565 9. DAHLGREN 5, NORDENSTROM B: Transthoracic Needle Biopsy, Year Bk Med, Chicago, 1966 10. LALLI AF: The direct fluoroscopically guided approach to renal, thoracic and skeletal lesions. Curr Probi' Radiol 2: 1, 1972 11. HENDRY WE, WILLIAMS JP: Transrectal prostatic biopsy. Br Med J 4: 595, 1971 12. LuNDQUIsT A: Fine-needle aspiration biopsy of the liver. Applications in clinical diagnosis and investigation.
Acta Med Scand (Suppl]: no 520, 1971 13. OSCARSON J, STORMBY N, SUNDOREN R: Selective angiography in fineneedle aspiration cytodiagnosis of gastric and pancreatic tumors. A cia Ra-
diol [Diagn] (Stockh) 12: 737, 1972 14. HANCKE 5, HOLM HH, KocH F: Ultrasonically guided percutaneous fine needle biopsy of the pancreas. Surg
Gynecol Obstet 140: 361, 1975 15. HOLM HH, PEDERSEN JF, KRISTENSEN JK, et al: Ultrasonically guided percutaneous puncture. Radiol Clin North Am 13: 493, 1975 16. TYLEN U, ARNESJO B, LINDBERG LG, et al: Percutaneous biopsy of carcinoma of the pancreas guided by angio-
graphy. Surg Gynecol Obstet 142: 737, 1976 17. GOLDSTEIN HM, ZORNOZA J, WALLACE 5, et al: Percutaneous fine needle aspiration biopsy of pancreatic and other abdominal masses. Radiology 123: 319, 1977 18. ZORNOZA J, JoNsso. K, WALLACE S, et al: Fine needle aspiration biopsy of retroperitoneal lymph nodes and abdominal masses: an updated report.
Radiology 125: 87, 1977 19. Ho C-S, MCLOUGHLIN MJ, MCHATTIE JD, et al: Percutaneous fine needle aspiration biopsy of pancreas following endoscopic retrograde cholangiopancreatography. Ibid, p 351 20. MCLOUGHLIN MJ, Ho C-S, LANGER B, et al: Fine needle aspiration biopsy of malignant lesions in and around the pancreas. Cancer 41: 2413, 1978 21. SMITH IH, FISHER JH, Lorr JS, et al: The cytological diagnosis of solid tumours by small needle aspiration and its influence on cancer clinic practice.
Can Med Assoc J 80: 855, 1959 22. ENGZELL U, JAKOBSSON PA, SIGIJRD-
24. STAVRIC GD, TEVCEV DT, KAFTAND-
JIEV DR, et al: Aspiration biopsy cytologic method in diagnosis of breast lesions: a critical review of 250 cases. Acta Cytol (Baltimore) 17: 188, 1973 25. KLINE TS, NEAL HS: Needle aspiration of the breast - why bother? Acta Cytol (Baltimore) 20: 324, 1976 26. ZAJDELA L, GHossEIN NA, PILLERON
JP, et al: The value of aspiration cytology in the diagnosis of breast cancer: experience at the Fondation Curie. Cancer 35: 499, 1975 27. FURNIVAL CM, HUGHES HE, HOCKING MA, et al: Aspiration cytology in breast cancer. Its relevance to diagnosis. Lancet 2: 446, 1975 28. ABRAHAMSON DJ: A clinical evaluation of aspiration of cysts of the breast. Surg Gynecol Obstet 139: 531, 1974 29. LAUBY VW, BURNETr WE, ROSEMOND GP, et al: Value and risk of biopsy of pulmonary lesions by needle aspiration. Twenty-one years' experience.
J Thorac Cardiovasc Surg 49: 159, 1965 30. STEVENS GM, WEIGEN iF, LILLINCTON GA: Needle aspiration biopsy of localized pulmonary lesions with amplified fluoroscopic guidance. Am J Roentgenol Radium Ther Nuci Med 103: 561, 1968 31. SANDERS DE, THOMPSON DW, PUDDEN BJE: Percutaneous aspiration lung
biopsy. Can Med Assoc J 104: 139, 1971 32. SARGENT EN, TURNER AF, GORDONSON J, et al: Percutaneous pulmonary needle biopsy: report of 350 patients. Am J Roentgenol Radium Tlaer Nuci Med 122: 758, 1974 33. ZORNOZA J, SNOW J JR, LUKEMAN JM.
et al: Aspiration biopsy of discrete pulmonary lesions using a thin needle. Results in the first 100 cases. Radiology 123: 519, 1977 34. FERGUSON RS: Diagnosis and treatment of early carcinoma of the prostate. J Urol 37: 774, 1937 35. ANDERSSON K, JONSSON G, BRUNK U: Puncture biopsy of the prostate in the diagnosis of prostatic cancer. Scand
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sies. Acta Cytol (Baltimore) 11: 470, 1967 46. SCHAJOWICZ F, DERQUI JC: Puncture biopsy in lesions of the locomotor system: review of result in 4050 cases, including 941 vertebral punctures. Cancer 21: 531, 1968 47. AKERMAN
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mours. I Laryngol Otol 90: 253, 1976 50. Es.osri P-L, EL MAN A, NORLEN H: Complications of transrectal biopsy of the prostate. Scand I Urol Nephrol 9: 208, 1975 51. STORMBY N, AKERMAN M: Aspiration
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L, et al: Fine needle and open biopsy in thyroid disorders. Acta C/dr Scand 141: 20, 1975 44. MAVEC P, ENEROTH C-M, FRANZEN 5, et al: Aspiration bio.psy of salivary gland tumours. 1. Correlation of cytologic reports from 652 aspiration biopsies with clinical and histologic findings. Acta Otolaryngol (Stock/i) 58: 471, 1964
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1328 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119
metastasis after percutaneous transthoracic needle aspiration biopsy. Acta
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et al: Investigation on tumour spread in connection with aspiration biopsy. Acta Radiol [Ther] (Stock/i) 10: 385, 1971 57. SNYDER RE, COLEY BL: Further studies on the diagnosis of bone tumors by aspiration biopsy. Surg Gynecol Obstet 80: 517, 1945 58. BERG JW, ROBBINS GF: A late look at the safety of aspiration biopsy. Cancer 15: 826, 1962 59. VON SCHREEB T, ARNER 0, SKOvSTED G: Renal adenocarcinoma. Is there a risk of spreading tumour cells in diagnostic puncture? Scand I Urol Nephrol
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