EUROPEAN JOURNAL OF
ELSEVIER
European Journal of Ultrasound 2 (1995) 199-203
Clinical paper
Ultrasound-guided fine-needle aspiration of abdominal masses: Accuracy and short-term complications Janek Binek *a, Peter Spieler b, Rainer Hfirlimann a, Lidia Zoebeli b, Bruno Hammer a aGastroenterology Unit, Medizinische Klinik C, Kantonsspital, CH-9007 St. Gallen, Switzerland bDepartment of Cytopathology, Institute of Pathology, Kantonsspital, CH-9007 St. Gallen, Switzerland Received l0 August 1994; revision received 24 February 1995; accepted 5 March 1995
Abstract
Objective: To assess prospectively the sensitivity, specificity and short-term complications (24 h) of fine-needle ultrasound-guided punctures (FNA) of abdominal tumors. Methods: Fine-needle punctures were taken in 102 patients (188 needle passes) and after preparation the aspirate was examined by two experienced pathologists. Results: the sensitivity in detecting malignancy was 91.7% and the specificity ! 00%. The negative predictive value was 78.5%, the positive predictive value 100% and the overall accuracy 93.6%. We did not find an association between true positive or true negative results and the macroscopic appearance of the smear or the size of the punctured lesion. The minor complications rate was 3.9% (2.1% per needle pass), with no major complications. Conclusion: FNA of abdominal masses is a safe diagnostic procedure, with high specificity and sensitivity in detecting malignancies. Keywords: Ultrasound-guided puncture; Fine-needle; Abdominal tumor; Diagnostic accuracy; Complication; Short-term
1. Introduction
Fine-needle aspiration (FNA) is a commonly used procedure to assess the nature of suspected malignant lesions. Ultrasound-guided puncture is, in experienced hands, an easy, quick and cheap procedure. In collaboration with a skilled cytopathologist, a rapid and accurate diagnosis can be * Corresponding author.
achieved. Since 1980, 3000 abdominal ultrasound examinations are performed at our institution each year. The number of FNAs is 80/year. To assess our results a prospective study was designed. We wanted to evaluate the sensitivity, specificity and predictive values in detecting malignancy in focal abdominal lesions, and in the frequency of shortterm complications of the FNA. A further aim was to evaluate if patients could be discharged from the hospital 2 h after the procedure.
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J. Binek et aL /European Journal of Ultrasound 2 (1995) 199-203 A~
2. Materials and methods
A total of 102 hospitalized patients (45 women, 44.1%; 57 men, 55.9%) having a diagnostic FNA from January 91 to April 1992 were prospectively enrolled in the study. The mean age of the patients was 65 years (range 24-86 years). We used a 22 gauge non-cutting needle (Chiba Needle/M.S., 0.7 mm diameter, 15 era or 22 em length, with stylet). We did not employ a steering needle. Minimum requirements for coagulation parameters were a platelet count of > 50 x 109/1 and prothombin values of > 50% (INR > 1.6). We did not use local anaesthesia or analgesic drugs. The USguided puncture procedure was performed by two operators. All procedures were performed with the participation of at least one experienced operator. After skin disinfection, a linear probe (4 MHz) with a central needle guide was positioned by one examiner while the other one performed the puncture. We tried to place the needle tip in the peripheral region of the target lesion. Location and size of the lesion as well as the macroscopic appearance of the obtained sample were recorded. If the smear macroscopically did not appear to be cell-rich (i.e. bloody, no greyish cell aggregations), additional passes were performed immediately. A total of 180 needle passes was performed. In 44 (43.1%) patients only one, in 38 (37.2%) two and in 14 (13.7%) three needle passes were done. Only 5 and 1 subjects needed four and six needle passes, respectively (Fig. 1). The aspirated material was expelled in single drops on glass slides and immediately spray-fixed. Smears were then prepared for Papanicolaou stain. Whenever macroscopically sufficient material was obtained at least one smear was air dried for May-Griinwald-Giemsa stain. Immunocytochemical reactions were performed on Papanicolaou-stained smears to differentiate between epithelial and other cell types (i.e. stromal, lymphatic or tumor cells) and to recognize certain tumor types such as hepatoma or neuroendocrine tumors or to identify the origin of eventual metastases. Aspirated fluid was centrifuged and direct cell films were prepared from the sediment, followed by immediate fixation in Delaunay's fixative and stained according to Papanicolaou. Aspirates were evaluated by two ex-
Ckl 0 II C
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NEEDLE PASSES Fig. 1. Number of needle passes per patient (n = 188). perienced cytopathologists and reported as benign, suspicious (suggestive of malignant neoplasm), malignant or inconclusive. With a Fisher exact test, we investigated if macroscopically cell-rich smears were a reliable predictor of true or false results. A possible association between size of the lesions (range 0.5-13 cm) and true or false results was also examinated with a Fisher exact test (Dean et al. 1990). The median value of 4 cm was used for separating 'big' from 'small' lesions. Short-term complications were recorded immediately. For local pain assessment a visual analogue scale was used ('0' = no pain, '+' slight pain, '++' moderate pain, '+++' severe pain). Twentyfour hours after the puncture, complications were registered on a clinical basis; a control ultrasound was not performed. Complication rates were calculated per patient and also single needle pass. When the same patient was punctured in two or more sessions, every session was considered as a single event for calculating sensitivity and specificity. For calculating specificity and sensitivity the following criteria were used: cytological results classified as malignant and probably malignant are given as true positive, and benign as true negative. Furthermore, the cytological diagnosis of true positive results was confirmed by other methods such as histological examination of the whole lesion ob-
J. Binek et al./ European Journal of Ultrasound 2 (1995) 199-203
tained at surgery or autopsy. False negative results were confirmed by biopsy (taken by cutting needle biopsy, surgery or at autopsy). When an histological examination of the suspected lesion was not performed (often in the true negative patients) we followed the patient with repeated ultrasounds or CT scan, detecting change in the size and number of the lesions but also recording clinical and laboratory examinations (as tumor markers level in serum). The positive and negative predictive values were also calculated. Insufficient aspirates were considered only in the analysis of pain intensity and complications but not for calculating sensitivity, specificity and predictive values. 3. Results
The cytological analysis revealed in 67 patients (65.6%) a malignant (n = 63) or probably malignant (n = 4) and in 22 (21.5%) a non-malignant lesion. Six aspirates were classified as benign, but histological examination revealed malignancy. In 7 aspirates the cell sample was not representative. So we had 67 true positive, 22 true negative and 6 false negative. We did not have false positive resuits. The follow-up of true negative lesions was 10.5 months (median value, range 7-22 months). Specificity, sensitivity and predictive values are summarized in Table 1. Sensitivity in particular sites (at least 10 patients) was as follows: liver 87.8%, pancreas 84.6% and retroperitoneum 85.7% Table I Results of FNA in 102 patients No. of Patients True positive False positive True negative False negative Inconclusive aspirates Total
67 0 22 6 7 102
Specificity Sensitivity Positive predictive value Negative predictive value Overall accuracy
100 % 91.7% 100 % 78.5% 93.6%
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Table 2 Anatomical localization of puncture sites, sensitivity and specificity of the FNA at different Iocalisations ( ~ 10 patients) Puncture site
Patients
Sensitivity
Specificity
Liver Pancreas Retroperitoneum
49 (51.5%) 20 (21%) 14 (14.7%)
87.8% 84.6% 85.7%
100% 100% 100%
(see Table 2). A macroscopically cell-rich looking smear is not a reliable predictor for a right diagnosis (p = 1.0). We did not find an association between the size of the punctured lesions (_< 4 or > 4 cm) and true or false results (p = 0.205). Pain intensity due to the puncture was rated as '0' by 7, '+' by 42, '++' by 46 and '+++' by 7 patients. During the first 24 h, only one patient developed a subcutaneous haematoma. He had only one needle pass. Three other patients (all with 1 needle pass) had pain with an intensity of '+', that lasted more than 2 h. The overall minor complications rate was 3.9% (2.1% considering the single needle passes). Major complications of the FNA were not observed. 4. Discussion
In the literature the sensitivity of ultrasoundguided FNA (22-23 gauge) of abdominal masses ranges from 80% to 93% and the specificity from 98% to 100% (Droese et al. 1984; Smith and Butler 1988; Holtkamp et al. 1990). The sensitivity of FNA of liver lesions in studies enrolling more than 100 patients is 83%-95% (Schwerk et al. 1983; Otto 1985; Gebel et al. 1986; Hohkamp et al. 1990; Edoute et al. 1992). Comparable results (Sensitivity 69%-95%) were found in studies that considered only hepatocellular carcinoma (Bret et al. 1988; Buscarini et al. 1987; Bru et ai. 1989). Tumors of the pancreas can be punctured with a sensitivity between 81% and 90.6% (Otto 1985; Taavitsainen et al. 1987; A1-Kaisi and Siegler 1988; Sch6nenberg et al. 1990). Focusing on these two organs, we reached a similar sensitivity in our institution, without performing a rapid cytologic staining technique. A bedside cytological examination has been found to increase the sensitivity by allowing
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to repeat the FNA immediately if the aspirate is not representative (Civardi et al. 1988). We found that the macroscopic appearance of the smear does not represent a good alternative in evaluating the quality of the aspirate. We could not confirm that big lesions ( > 4 cm) were associated with better results. This does not seem surprising as other factors, such as experience of the doctor performing the punction, compliance and obesity of the patient, localization and histological peculiarities of the lesion influence the results. In this study, complications in the first 24 h after the puncture were not serious and rare. We believe, as we did, that every single needle pass should be considered separately, because every percutaneous needle pass is susceptible to cause complications. In one big retrospective Italian review of punctures with cutting (C) and non-cutting (NC) needles of less then 1 mm diameter two lethal events were reported (0.018%). Major complications have been observed in 0.18% of the cases but it is not described if a C or NC needle was used (Fornari et al. 1989). In another Danish series fineneedle biopsy aspiration (C, 0.6-0.8 mm and NC, 0.6 mm needle) the complication rate was 0.20% and the mortality rate 0.029% (Nolsoe et al. 1990). In a review of the incidence of complications assessed with questionnaires (Smith 1991) the mortality of FNA in Germany, Italy and USA ranged from 0.006% to 0.031% (Smith 1984; Weiss et al. 1988; Fornari et al. 1989; Smith 1991). Lethal haemorrhage is described even 2~, and 28 days, respectively, after puncture of adrenal pheochromocytoma and hepatic hemangioma (McCorkel and Niles 1985; Terriff et al. 1990). However, in many institutions, as is the case in our hospital, the punctures are also done on an outpatient basis (Bernardino 1984; Verbanck et al. 1994). Our low complication rate is also a consequence of our procedure policy: e.g. we tried not to puncture lesions on the surface of the liver, in the spleen or suspicious hemangiomas, as other centres do (Solbiati et al. 1985; Siniluoto et al. 1992). Other observed contra-indications were an abnormal haemostasis, marked immunosuppression and tense ascites (Yeung 1992).
Our study confirmed that FNA of abdominal organs can be performed with good sensitivity, negative predictive value and acceptable safety. As expected, specificity and positive predictive values were 100%. This combination of high sensitivity and a low complication rate make this method the procedure of choice in clarifying the etiology of focal abdominal lesions, The FNA is a procedure that can also be done on an outpatient basis. References AI-Kaisi N, Siegler EE. Fine-needle aspiration cytology of the pancreas. Acta Cytol 1988; 33: 145-152. Bernardino ME. Percutaneous biopsy. Am J Roentgenol 1984; 142: 41-45. Bret P, Labadie M, Bretagnolle M, Paliard P, Fond A, Valett PJ. Hepatocellular carcinoma: diagnosis by percutaneous fine-needle biopsy. Gastrointest Radiol 1988; 13: 253-255. Bru C, Maroto A, Bruix J, Faus R, Bianchi L, Calvet X, Ayuso C, Vilana R, Gilabert R, Rodes J. Diagnostic accuracy of fine-needle aspiration biopsy in patients with hepatocellular carcinoma. Dig Dis Sci 1989; 34: 1765-1769. Buscarini L, Sbolli G, Cavanna L, Civardi G, Di Stasi M, Buscarini E, Fornari F. Clinical and diagnostic features of 67 cases of hepatocellular carcinoma. Oncology 1987; 44: 93-97. Civardi G, Fornari G, Cavanna L, Di Stasi M, Sbolli G, Buscarini L. Value of rapid staning and assesment of ultrasound-guided fine-needle aspiration biopsies. Acta Cytol 1988; 32: 552-554. Dean AG, Dean JA, Burton AH, Dicker RC. Epi lnfo, Version 5: a word processing, database, and statistics program for epidemiology on microcomputers. USD Incorporated, Stone Mountain, Georgia, 1990. Droese M, Altmannsberger M, Kehl A, Lankisch PG, Richard W, Weber K, Osborn M. Ultrasound-guided percutaneous fine-needle aspiration biopsy of abdominal and retroperitoneal masses. Acta Cytol 1984; 28: .368-384. Edoute Y, Tibon-Fisher O, Ben Haim S, Malberger E. Ultrasonically-guided fine-needle aspiration of liver lesions. Am J Gastroenterol 1992; 87:1138-1141. Fornari F, Civardi G, Cavanna L, Di Stasi M, Rossi S, Sbolli G, Buscarini L and the cooperative Italian Study Group. Complications of ultrasonically-guided fine-needle abdominal biopsy. Scand J Gastroenterol 1989; 24: 949-955. Gebel M, Horstkotte H, Kister C, Brunkhorst R, Brandt M, Atay Z. Ultraschall-gezielte Feinnadelpunktion abdomineller Organe: lndikationen, Ergebnisse, Risiken. Ultraschall 1986; 7: 198-202. Holtkamp W, Thelmeier A, Droese M, Ebert R, Reis HE. Ultraschallgesteruerte Feinnadelpunktion. Dtsch Med Wochenschr 1990; 115: 809-812. McCorkel SJ, Niles NL. Fine-needle aspiration biopsy of catecholamine-producing adrenal masses: a possibly fatal mistake. Am J Roentgenol 1985; 145: 113-114.
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