Percutaneous fineneedle aspiration biopsy of intra*abdominal masses CHIA-SING Ho, MB, BS, FRCP[C]; LIANG-CHE TAO, MD, FRCP[C]; MICHAEL J. MCLOUGHLIN, MB, BS, MRCP (LOND), FRCR, FRCP[C]

Percutaneous fine-needle aspiration biopsies were performed in 51 patients with various intra-abdominal masses localized by palpation, radiologic studies, ultrasonography or radioisotope scanning. Biopsy specimens were considered positive for malignant disease in 35 (850/c) of the 41 patients with such disease, including 26 (960/o) of the 27 with metastases. There was one false-positive diagnosis of malignant disease from the biopsy specimens. Surgery became unnecessary as a result of aspiration biopsy in at least 12 patients. One patient showed evidence of intrahepatic bleeding during liver biopsy but recovered spontaneously, and the liver appeared normal at laparotomy 3 weeks later. Aspiration biopsy is an accurate, relatively painless, inexpensive and safe method of establishing a diagnosis of intra. abdominal malignant disease. Consider. able experience of the cytologist is necessary for good results.

Needle aspiration has been used for many years in the biopsy of superficial lesions (e.g., superficial lymph nodes and breast lumps),1-3 the prostate4'5 and the lung.64 Biopsy may also be done in this way on intraabdominal organs including spleen,9-12 kidney,13-17 liver,17-20 pancreas21 -27 and retroperitoneal lymph nodes.28'29 We have previously described our experience with the biopsy of lesions in and around the pancreas,.'27'30 and in this paper we describe the findings in 51 patients undergoing transabdominal fine-needle aspiration biopsy for various other lesions between November 1976 and April 1978 at our hospital. Methods Patients and biopsy site In 51 patients 56 biopsies were performed; 5 patients had repeat biopsies because the results of the Des biopsies par aspiration percutan6e first were inconclusive. The patients' a l'aiguille fine ont et6 pratiquees ages ranged from 23 to 79 (average chez 51 patients pr6sentant diverses 60) years. The regions and organs masses intra-abdominales localisees par palpation, etudes radiologiques, thus examined are summarized in ultrasonographie ou scintigraphie Table I. The patients were supine isotopique. Les biopsies ont ete trouv6es for 47 biopsies and prone for 9. positives pour une maladie maligne The patients received no special chez 35 (850/o) des 41 patients souffrant preparation. dune telle maladie, y compris 26 (960/c) des 27 patients ayant des Localization of lesion metastases. II y a eu un faux resultat Prior to biopsy the lesion was lopositif de biopsie par aspiration calized either by palpation or by repercutan6e. GrAce a Ia biopsie par view of radiologic studies, ultrasonoaspiration l'intervention chirurgicale a grams or radioisotope scans (Table pu Atre 6vitee chez au moms 12 patients. Un patient a montre des signes II). In some cases the lesion was d'hemorragie intrahepatique pendant Ia evident fluoroscopically - for exbiopsie du foie mais ii sest r6tabli ample, when contrast material was spontan6ment et le foie est apparu found in lymph nodes following lymnormal a Ia laparotomie 3 semaines phography. In others, such as cases plus tard. La biopsie par aspiration est of renal and pelvic lesions, localizaune m6thode pr6cise, relativement tion was aided by prior intravenous indolore, peut coOteuse et sOre d'6tablir un diagnostic de maladle intra. abdominale maligne. Le cytologiste doit posseder une vaste experience pour obtenir de bons resultats.

for the biopsy needle, usually directly over the lesion, was marked on the skin. Biopsy The skin and tissues down to the peritoneum were locally anesthetized, and a small incision was made in the skin with the point of a scalpel to facilitate introduction of the 22- or 23-gauge spinal needle used for biopsy. The needle and stylet were passed through the body wall, the stylet was removed and the needle was advanced into the lesion. When tumour was present firm resistance was usually felt at the needle tip, and occasionally the needle could be advanced and withdrawn only with difficulty. The needle was moved backwards and forwards and rotated in the lesion, and intermittent suction was applied with a well-fitting syringe to detach material in the needle from surrounding tissues. Following withdrawal of the needle the material was blown out of the needle onto

injection of urographic contrast material. When neither method was

available the lesion was located by reference to bony landmarks at the time of fluoroscopy. The entry point

From the departments of radiology and pathology, Toronto General Hospital Reprint requests to: Dr. Chia-Sing Ho, Department of radiology, Toronto General Hospital, 101 College St., Toronto, Ont. MSG 1L7 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1311

slides with an air-filled syringe. Thin smears were made and fixed in alcohol immediately, while wet, for subsequent staining by the PapanicoIaou method. Two or three aspirations were usually done with the direction of the needle changed, and a dozen or more slides were prepared. Biopsy specimens were considered positive for malignant disease only when unequivocally malignant cells were detected. Specimens with suggestive or highly suggestive findings were considered negative. Results

The final diagnoses in the 51 patients, the number in whom the diagnosis was confirmed by other methods and the number with biopsy specimens positive for malignant disease are shown in Table III. Among the aspiration biopsy diagnoses 35 were true-positive, 9 true-negative, 6 falsenegative and 1 false-positive. In the last instance hepatic malignant disease was erroneously diagnosed from scanty material in a patient with cirrhosis. Overall, aspiration biopsy specimens were positive for malignant disease in 35 (85%) of the 41 patients with such disease. Aspiration biopsy was particularly valuable in the diagnosis of metastases anywhere in the abdomen (carcinoma in all cases), yielding positive specimens in 26 (96%) of the 27 patients with metastases. Because these results were well accepted, proof of the diagnosis was obtained by other means in only six instances; there was no reason to doubt the diagnosis in any of the other patients. Primary malignant tumours had been diagnosed in 15 patients 6 months to 14 years previously; in the other 12, metastases were diagnosed when the patient first presented for assessment. In most instances the cytomorphologic features were consistent with those of the known primary tumour or they suggested the origin of the primary when this was unknown. The results were poorer in the diagnosis of primary malignant disease: aspiration biopsy specimens were positive in only 9 (64%) of all 14 patients and in only 4 of the 8 with primary carcinoma. However, the number of cases was small, and several of the patients with primary carcinoma had been referred for

biopsy only because more conventional diagnostic methods had failed. Lymphoma was diagnosed from aspiration biopsy specimens in five patients, but could be classified in only three. Four of these patients were new and had undiagnosed retroperitoneal masses. Treatment was started on the basis of the aspiration results in two, but operative biopsy was required in the other two. In the fifth patient aspiration biopsy was used to confirm retroperitoneal disease in a patient with known lymphoma and equivocal lymphographic changes. Aspiration biopsy was of no assistance in patients with benign lesions, except that it tended to exclude malignant disease. In two patients very useful information was obtained even though a complete diagnosis was not made from the biopsy specimens. In a patient with a suprarenal mass an adrenal cortical tumour (benign or malignant) was diagnosed by cytology; an operation revealed an invasive adrenal cortical carcinoma. In

1312 CMA JOURNAL/DECEMBER 9, 1978/VOL. 119

another patient with an adrenal mass the clear fluid aspirated contained no malignant cells; when injected contrast material demonstrated a smooth-walled cyst, a diagnosis of benign adrenal cyst was made and an operation avoided.31 Biopsy specimens falsely negative for malignant disease were obtained in five other patients. The first had a large retroperitoneal mass indenting the colon; although aspiration biopsy yielded only acute inflammatory cells, an operation disclosed a large paracolic abscess and an underlying carcinoma of the colon. In the second, an 18-year-old man, a large renal mass was found at the time of operation to be largely hemorrhagic; microscopically renal carcinoma cells were noted peripherally. The third patient was found surgically to have metastatic adenocarcinoma in the liver; biopsy material had been scanty and reported as "highly suggestive of adenocarcinoma". Although in the fourth patient the biopsy needle was seen fluoroscopically to be within a

parosteal sarcoma of the ilium, tumour cells were not present in the scanty material aspirated. In the fifth patient, a 68-year-old man who was thought clinically and angiographically to have hepatoma throughout the liver, and who subsequently died, the liver aspiration biopsy specimens were negative for malignant disease, although adequate material was obtained. From this we conclude that falsenegative results of aspiration biopsy are usually due to failure to obtain material containing malignant cells. This may be because the needle misses the lesion completely or because the lesion is nonhomogeneous (e.g., necrotic or hemorrhagic) or, rarely, because tumour cells are not aspirated even when the needle is well placed. Only one patient in this series experienced complications: pain, tachycardia and hypotension occurred during a liver biopsy, the hemoglobin concentration fell by 1 g and small lucencies attributed to hematoma were noted in a subsequent computed tomographic scan of the liver. The patient recovered spontaneously and the liver appeared normal at laparotomy 3 weeks after the biopsy. The effect of biopsy on the overall management of the patients was difficult to assess; it varied from confirmation of a clinical impression to a significant alteration in treatment. An operation became unnecessary as a result of biopsy in at least 12 of the 51 patients. Discussion Our findings, and those of others,.'2' have indicated clearly that percutaneous fine-needle aspiration biopsy is an excellent method of confirming a diagnosis of intra-abdominal malignant disease, particularly metastatic carcinoma. It is highly accurate, yielding few false-negative and fewer false-positive results, and it is relatively painless, safe and inexpensive. It is indicated early in the assessment of an abdominal mass in many patients with malignant disease or a history of malignant disease when positive results may obviate other investigations, including surgical exploration. Although not widely used for diagnosing malignant disease of the liver, aspiration biopsy has been shown to

be of value.'7'18-20 Biopsy specimens were positive in 57 (77%) of 74 such cases in Lundquist's study,18 and Hoim and colleagues17 showed ultrasonically guided aspiration biopsy to be more accurate than Menghini needle biopsy. We recommend fineneedle aspiration biopsy for the diagnosis of malignant disease of the liver. The needle can be aimed at a lesion located by radioisotope scanning or ultrasonography, a large volume of liver in both lobes may be sampled by altering the direction of the needle, and the risk is small. Renal masses are usually detected by intravenous pyelography, and most are renal cysts or, less commonly, renal cell carcinomas. Ultrasonography is useful to differentiate cystic from solid lesions. Cyst puncture may be used to confirm a diagnosis of renal cyst, and angiography will be diagnostic for most renal carcinomas. Renal cell carcinoma can also be diagnosed by aspiration biopsy,"'7 which yields positive results in 72% to 88% of cases.'4"5'17 Needle biopsy of all renal masses following intravenous pyelography and ultrasonography has been suggested either to confirm a diagnosis of renal cyst or to obtain material from tumours for cytologic examination.15"7 We believe that aspiration of renal masses is underused and is strongly indicated when the results of ultrasonography and angiography are inconclusive. Aspiration biopsy should also be performed when fluid is not obtained by attempted puncture of a presumed renal cyst. The diagnosis of intra-abdominal lymphoma can usually be made by aspiration biopsy, but accurate morphologic diagnosis is difficult. Excisional biopsy of an accessible lymph node for histologic examination is therefore preferred. Aspiration biopsy is helpful in patients with undiagnosed masses (usually retroperitoneal) whose disease appears to be limited to the abdomen, and occasionally to confirm a diagnosis of intraabdominal recurrence in a patient with previously diagnosed lymphoma. Transabdominal aspiration biopsy should be performed with fine needles (22- or 23-gauge) to reduce the possibility of complications. mitially we tried the 23-gauge Chiba ("skinny") needle, which was devised for percutaneous transhepatic cholangiography and is highly flexible.'2

For biopsy it proved to be too flexible, tending to bend or deflect when a tumour mass was encountered. We now use standard 22-gauge spinal needles of suitable length, which are more rigid. We do most aspirations with the patient supine, except in the case of renal and perirenal masses, which are aspirated with the patient prone. The position appears to have no effect on the results of biopsy or on the rate of complications. Biopsy may be repeated if the results are inconclusive. In a few patients - often those with large tumours - aspiration biopsy is painless. Most, however, have transient discomfort. Two patients in our series, one with a large paraspinal neurilemoma and one with recurrent cervical carcinoma involving sacral nerve roots, had severe pain. Although in many biopsies the needle passes through various hollow and solid viscera and vascular structures, this is of little consequence. The fine needle is approximately 14 times smaller in cross-sectional area than a Silverman needle,27 and in animals subjected to laparotomy following biopsy the puncture sites usually cannot be seen.'."' Similarly, in most patients undergoing an operation after biopsy, no abnormalities are observed,25".'27"' although occasionally a small asymptomatic hematoma is found 15.l7,24.25.27

Complications from transabdominal fine-needle aspiration biopsy are rare. Stormby and Akerman5' found none in more than 1000 aspirations of the liver, and S6derstrom'2 found none in a similar number of splenic biopsies. Lundquist" encountered one complication (intrahepatic hematoma requiring surgical evacuation) in 2611 liver aspirations. Single instances of biliary peritonitis after liver aspiration's and pancreatitis after pancreatic biopsy27 have also been reported. The only associated death of which we are aware was due to intraperitoneal hemorrhage following liver aspiration in a patient with cirrhosis, hepatoma and liver failure." The possibility of seeding of the needle track with tumour cells following needle biopsy is often raised. However, as we have pointed out elsewhere,27 such seeding is rare and almost invariably follows punch biopsy with large-bore needles, most com-

CMA JOURNAL/DECEMBER 9, 1978/VOL. 119 1313

monly in transperineal biopsy of the prostate with a Silverman needle. There is only one documented case of tumour recurrence in the needle track following aspiration biopsy.36 Widespread dissemination of tumour cells by biopsy, with reduced survival, is also theoretically possible, but is difficult to assess. Shortened survival could not be demonstrated in groups of patients undergoing aspiration biopsy for osteogenic sarcoma37 or cancer of the breast,38 kidney39 or lung. Transabdominal aspiration biopsy is contraindicated in patients with hemorrhagic diathesis and whenever there is a possibility of hydatid disease. The technique of fine-needle aspiration biopsy is easily learned, but considerable experience of the cytologist is necessary for good results. References 1. STEWART FW: The diagnosis of tumors by aspiration. Am J Pathol 9 (suppi): 801, 1933 2. MARTIN HE, ELLIS EB: Aspiration

biopsy. Surg Gynecol Obstet 59: 578, 1934 3. Ess'os.n P-b, FRANZEN 5, ZAJICEK J: The aspiration biopsy smear, in Diagnostic Cytology and its Histopathologic Bases, vol 2, Koss LG, DURFEE

13. VON SCHREEB T, FRANZEN 5, LJUN-

OQYIST A: Renal adenocarcinoma. Evaluation of malignancy on a cytologic basis: a comparative cytologic and histologic study. Scand J Urol Nephrol 1: 265, 1967 14. ALFTHAN 0, KoIvUNIEMI A: Percu-

taneous cytological aspiration biopsy in the diagnosis of renal tumours. Ann Chir Gynaecol Fenn 58: 304, 1969 15. KRISTENSEN JK, HOLM HH, RASMUS-

SEN SN, et al: Ultrasonically guided percutaneous puncture of renal masses. Scand J Urol Nephrol 6 (suppl 15): 49, 1972 16. LALLI AF: The direct fluoroscopically guided approach to renal, thoracic and

skeletal lesions. Curr Probi Radio! 2: 1, 1972 17. HOLM HH, PEDERSEN JF, KRISTENSEN

JK, et al: Ultrasonically guided percutaneous puncture. Radio! Clin North Am 13: 493, 1975 18. LUNDQUJST A: Fine-needle aspiration biopsy of the liver. Applications in clinical diagnosis and investigation. Acta Med Scand [Suppi]: no 520, 1971 19. JOHANSEN 5, MYREN J: Fine-needle

aspiration biopsy smears in the diagnosis of liver diseases. Scand J Gastroenterol 6: 583, 1971

Radiology 125: 87, 1977 30. TAO L-C, Ho C-S, MCLOUGHLIN MJ, et al: Percutaneous fine needle aspiration biopsy of the pancreas: cytodiagnosis of carcinoma of the pancreas. Acta Cytol (Baltimore) 22: 215, 1978 31. SCHEIBLE W, COaL M, SIEMERS PT, et al: Percutaneous aspiration of adrenal cysts. Am J Roentgenol 128: 1013, 1977 32. OKUDA K, TANIKAWA K, EMURA T, et al: Nonsurgical, percutaneous transhepatic cholangiography - diagnostic significance in medical problems of the liver. Am I Dig Dis 19: 21, 1974 33. STORMBY N, AKERMAN

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tion cytology in the diagnosis of granulomatous liver lesions. Acta Cytol (Baltimore) 17: 200, 1973 34. SCHULZ TB: Fine-needle aspiration biopsy of the liver complicated with bile peritonitis. Acta Med Scand 199:

141, 1976 35. RIssc. H, FRIMAN C: Fatality after fine-needle aspiration biopsy of liver (C). Br Med 1 1: 517, 1975 36. SINNER WN, ZAJICEK J: Implantation metastasis after percutaneous transthoracic needle aspiration biopsy. Acta

Radiol [Diagn] (Stockh) 17: 473, 1976 37. SNYDER RE, COLEY BL: Further

20. RASMUSSEN SN, HOLM HH, KRISmNSEN JK, et al: Ultrasonically-guided

studies on the diagnosis of bone tumors by aspiration biopsy. Surg Gyneccl Obstet 80: 517, 1945

liver biopsy. Br Med J 2: 500, 1972

38. BERG JW, ROBBINS GF: A late look

21. OSCARSON J, STORMBY N, SUNDOREN

at the safety of aspiration biopsy. Cancer 15: 826, 1962

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J Thorac Cardiovasc Surg 49: 159, 1965 7. D.AHLGREN 5, NORDENSTROM B: Trans-

thoracic Needle Biopsy, Year Bk Med, Chicago, 1966 8. LALLI AF, MCCORMACK U, ZELCH M, et al: Aspiration biopsies of chest lesions. Radiology 127: 35, 1978 9. MOESCHLIN S: Spleen Puncture, PINEY A (trans), Heinemann, London, 1951 10. MORRIsoN M, SAMWICK AA, RUBINSTEIN J, et al: Splenic aspiration. Clinical and hematologic considerations based on observation in 105 cases.

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29. ZORNOZA J, JONSSON K, WALLACE 5, et al: Fine needle aspiration biopsy of retroperitoneal lymph nodes and ab-

HARRISON'S PRINCIPLES OF INTERNAL MEDICINE. 8th ed. Edited by George W. Thorn, Raymond D. Adams, Eugene Braunwald and others. 2088 pp. Illust. McGraw-Hill Book Company, New York; McGraw-Hill Ryerson Limited, Scarborough, Ont., 1977. $56.40. ISBN 0-07064519-1 (two-volume set) THE HEART. Arteries and Veins. 4th ed. Edited by J. Willis Hurst, R. Bruce Logue, Robert C. Schlant and others. 2022 pp. Illust. McGraw-Hill Book Company, New York; McGraw-Hill Ryerson Limited, Scarborough, Ont., 1978. $70.80. ISBN 0-07-031472-1 (two-volume set) THE METABOLIC BASIS OF INHERITED DISEASE. 4th ed. Edited by John B. Stanbury, James B. Wyngaarden and Donald S. Fredrickson. 1862 pp. IlIust. McGraw-Hill Book Company, New York; McGraw-Hill Ryerson Limited, Scarborough, Ont., 1978. $78. ISBN 0-07-060725-7 THE NEUROANATOMIC BASIS FOR CLINICAL NEUROLOGY. 3rd ed. Talmage L. Peele. 609 pp. lIlust. McGraw-Hill Book Company, New York; McGraw-Hill Ryerson Limited, Scarborough, Ont., 1977. $35.40. ISBN 0-07-049175-5

dominal masses: an updated report.

continued on page 1323

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piration biopsy of pancreatic and other abdominal masses. Radiology

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319, 1977 26. Ho C-S, MCLOUGHLIN MJ, MCHATTIE

JD, et al: Percutaneous fine needle aspiration biopsy of pancreas following endoscopic retrograde cholangiopancreatography. Radiology 125: 351, 1977 27. 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 28. GOmLIN JH: Post-lymphographic percutaneous fine needle biopsy of lymph nodes guided by fluoroscopy. Radiology 120: 205, 1976

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