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DOI:10.2214/AJR.08.1573
AJR 2008; 191:1649-1651
© American Roentgen Ray Society


Centennial Article

"Diagnosis of Abdominal Malignancy by Radiologic Fine-Needle Aspiration Biopsy"—A Commentary

Thomas B. Kinney1

1 Department of Radiology, University of California, San Diego, Medical Center, Interventional Radiology, 200 W Arbor Dr., San Diego, CA 92103-8756.

Received July 22, 2008; accepted after revision July 24, 2008.

Periodically, the American Journal of Roentgenology will republish online one of the 100 most-cited articles from its first century. A corresponding commentary in the journal by a contemporary radiologist will provide a current perspective. For a full list of these articles, see page 3 of the January 2006 issue of the AJR or go to www.ajronline.org. Centennial article series Guest Editor: Liem T. Bui-Mansfield, ARRS Figley Fellow 2004.

Address correspondence to T. B. Kinney (tbkinney{at}ucsd.edu).

Keywords: biopsy • coaxial biopsy

...it is reasonable to predict that within the near future diagnostic assessment of most abdominal masses will include an attempt at fine-needle aspiration biopsy as a routine preoperative maneuver. [1]

It was with extreme pleasure that I accepted the invitation from Liem T. Bui-Mansfield to provide commentary on this landmark AJR article by Ferrucci et al. [1] at Massachusetts General Hospital on the safety and efficacy of diagnosis of abdominal malignancy by radiologic fine-needle aspiration biopsy. This article is one of the 100 most-cited articles from the first century of publication of this prestigious journal.

I can recall the first time I read this article [1]. I was a medical student at the University of California, San Diego, and my faculty advisor was Skip vanSonnenberg, who referred me to the article. Because of that connection and the reputation of the radiology residency program at Massachusetts General Hospital, I was fortunate enough to obtain a position there. I was privileged to work first-hand with the first four authors of the article. I will always be eternally grateful for all the guidance and instruction they provided me.

Ferrucci et al. [1] conducted a retrospective review of 100 consecutive patients referred to the radiology department for fine-needle aspiration biopsies from 1975 to 1979. They realized that, although prior reports had described percutaneous needle biopsy techniques for hepatic, renal, and extraabdominal disorders, only recently had these methods been adapted for nonoperative confirmation of advanced or unresectable abdominal malignancy. They recognized that the confluence of three key refinements had allowed such technical advancement. The progress in new cross-sectional methods, such as sonography and CT, obviated surgical exploration. The fine-caliber 22- or 23-gauge, flexible, thin-walled Chiba needle developed for transhepatic cholangiography provided a wide safety margin. Finally, refinements in cytologic criteria and handling of thin-needle specimens permitted accurate diagnosis from small biopsy samples.

The indication for fine-needle aspiration was for low-risk, painless diagnosis of incurable or unresectable intraabdominal malignancy without need for laparotomy. The cases included presumed carcinoma of the body or tail of the pancreas; presumed cancer of the pancreatic head with evidence of local unresectability or distant metastases; presumed malignant biliary or ureteral obstruction; large, obviously unresectable, abdominal mass; focal liver masses; suspected intraabdominal metastases; lymph node metastases; and poor surgical risk. Contraindications for the procedure included uncooperative patients, uncorrectable coagulopathy, and highly vascular primary liver tumors (hepatocellular carcinoma and hemangioma).

The technique featured a 22-gauge Chiba needle with aspiration. The imaging techniques used were CT in 41 cases (41%), sonography in 45 cases (45%), and fluoroscopy with contrast enhancement in 14 cases (14%). The preferred and easiest approach was through the anterior abdominal wall, but posterior or flank approaches were used if they were shorter. Perpendicular orientation of the needle was also preferable but was not possible in all cases. Therefore, lesions of the superior right hepatic lobe were reached with a steep subcostal approach to avoid the costophrenic sulcus. After mild sedation, sterile preparation, and topical anesthetic, the needle was inserted with guidance and a sensation of tactile tumor resistance was often felt. No special efforts were made to avoid interposed bowel loops. If the mass was not entered with this needle, an adjusted insertion was made to sequentially converge on the targeted lesion. Ferrucci et al. [1] used a "tandem technique" to place additional needles as close to, and to the same depth as, the initial guide. This allowed quick, accurate access to the same target site without the necessity of repeated imaging. To minimize falsely negative biopsy from necrotic tumors, the authors used a guided multiquadrant approach to sample the tumor periphery when appropriate. Most of the samples consisted of cytologic smears, although some provided histologic material as well. The patients were observed for 4 hours after biopsy and discharged with a responsible individual.

Of the 84 patients ultimately found to have malignancy, aspiration cytology was positive in 69 (82%) patients. In the study, 86% of pancreatic neoplasms, 83% of liver neoplasms (usually metastases), and 78% of retroperitoneal lymph nodes were successfully identified. The overall success for epithelial malignancy was 85%, which far exceeded the yield with lymphomatous masses (40%). Falsely negative biopsies occurred in 15 such patients. Three had retroperitoneal lymphoma, three were necrotic, and nine cases were attributed to a geographic miss or to the scirrhous fibrotic nature of the tumor. In the 16 remaining patients who ultimately did not have cancer, surgery showed inflammatory processes in four patients in whom aspiration revealed purulent material, and 12 had no evidence of cancer with follow-up (1–35 months) after benign biopsy.

The influence of the number of needle passes was evaluated in a subgroup of 20 patients. In 75% of cases, the positive diagnosis occurred on the first needle pass. A small constant additional fraction of positive diagnoses was obtained in each successive needle pass. Generally, five passes were made. There were three complications (3%). One patient developed a pneumothorax from bilateral adrenal biopsy but required no treatment. Another patient developed shaking chills after pancreatic biopsy with positive blood cultures and was treated with antibiotics. This patient was thought to have biopsy through the bowel as a source of contamination. A third patient who required 10 needle passes to document pancreatic malignancy developed needle track seeding 3 months after biopsy.

Ferrucci et al. [1] concluded that "...percutaneous fine-needle aspiration biopsy is an accurate, safe, widely applicable method for pathologic diagnosis of deep abdominal neoplasms. Indeed, analogous to the accepted value of percutaneous lung biopsy and endoscopic biopsy of alimentary tumors, it is reasonable to predict that within the near future diagnostic assessment of most abdominal masses will include an attempt at fine-needle aspiration biopsy as a routine preoperative maneuver."

Since the publication of this landmark article [1], the application of biopsy techniques for intraabdominal mass lesions has certainly expanded. Advances in needle design have helped to improve diagnostic yield. In addition to the noncutting aspiration needles such as the Chiba, aspiration cutting needles such as the Turner and Franseen have circumferentially sharpened tips to enhance the yield of cytologic specimens that may provide microhistologic specimens as well [2]. Cutting needles can provide core samples for histologic examination and come in various sizes. The smaller caliber (18–20 gauge) cutting needles currently available provide high-quality histopathologic samples with few passes and infrequent complications. Indeed, the use of both fine-needle aspiration and core biopsy yields the highest success rates, indicating that the two methods are complementary [2, 3]. We prefer involvement of pathologists on site because this optimizes clinical correlation and ensures that specimens are optimally handled and sent for required ancillary investigations including microbiology or molecular studies.

Although Ferrucci et al. [1] used a tandem needle approach, many physicians currently prefer the coaxial technique. A thin-walled guide needle is carefully advanced with imaging guidance into the lesion. Through this needle, aspiration fine needles or coring needles can be advanced. This technique reduces patient discomfort and allows for additional passes to be made to retrieve more material for the pathologist. A modified coaxial method used a 23-gauge needle with a detachable hub that was advanced into the lesion; when the lesion was reached, the hub was removed and a 19-gauge needle was advanced over the first needle [4]. Biopsy was then performed with needles inside the 19-gauge needle. A special side-exiting needle guide was developed to aid multiquadrant biopsy, as referenced in the original article [5].

As Ferrucci et al. [1] mention, the shortest pathway from the skin to the lesion is preferred but not always possible. Many technical modifications have been reported to overcome the limitations. The triangulation method is used to biopsy out-of-plane cranial or caudal skin entry and has an angled approach for safe, effective needle placement [6]. Procedure planning and CT gantry angulation may be extremely helpful in such cases as well. Injection techniques may displace intervening structures to create a direct, safe pathway to the lesion [7, 8]. Using the Hawkins needle, which has a blunt trocar, may reduce injury to bowel, vessels, and nerves in difficult needle pathways [9]. Application of compression sonography to displace sensitive structures during intraabdominal mass biopsy provides access in certain situations [10, 11]. Use of a nonaspiration biopsy technique has also been advocated for biopsy of vascular lesions [12]. Custom-made curved needles have also been used to sample linearly inaccessible lesions [13, 14].

Although the guidance techniques described in the Ferrucci et al. [1] article are commonly used today, additional advances have occurred. CT fluoroscopy combines high-resolution CT with the real-time imaging capability of fluoroscopy [2]. This has been shown to reduce procedure time and the number of needle passes. The use of MRI guidance is advancing with the advent of open configuration MR systems, MR-compatible needles, and improved sequences [15]. The advantages of MRI guidance for biopsy include high contrast resolution, multiplanar imaging, vascular detail, lack of ionizing radiation, and 2D and 3D imaging. MRI may visualize lesions that remain occult with other techniques. Magnetic field–based electronic guidance systems have been developed as well [16]. Integrated PET/CT systems are extremely useful for planning lesion biopsy, with potential enhancement in yield using the procedure [2]. Contrast-enhanced sonography is useful for identifying hypervascular, potentially viable areas of lesions to increase biopsy efficacy [17]. Review of the article emphasizes to me the advances that have been made in imaging in the past two decades and also reinforces the interventional talents that these authors possessed to successfully perform the biopsies with the imaging capabilities available.

Complications from percutaneous biopsy of intraabdominal tumors remain acceptable [18]. Bowel traversal with small needles is usually safe [18, 19], but transgression of the colon should be avoided, particularly with large-bore needles. Biopsy of hypervascular primary lesions of the liver and even hemangioma is now considered safe [20]. Malignant needle track seeding is still a potential complication with biopsy at many sites. Recently, biopsies of small, incidentally discovered renal masses have been suggested as a method to reduce unnecessary surgery or ablative procedures [21]. The use of fine-needle biopsy and core biopsy in the diagnosis of lymphoma has improved significantly, with yields approaching 90%. The addition of core biopsy to fine-needle aspiration, the use of larger coring needles (20–14 gauge), and technical advances and close collaboration with pathologists have aided diagnosis of lymphoma and lymphoma recurrence [22]. Last, many biopsy procedures are performed as a prelude to focal ablative therapy, of which there are several forms including percutaneous injection (alcohol, acetic acid), thermal techniques (radiofrequency, microwave, and cryoablation), high-intensity focused sonography, and radioactive beads.

In conclusion, percutaneous biopsy of intraabdominal masses remains the mainstay in the workup of such lesions before therapy is considered. Because imaging techniques have improved, the diagnostic capabilities for characterizing lesions have reduced the need for some percutaneous biopsies. Hopefully, future advancements in diagnostic imaging will allow further specificity in regard to diagnosis and subtype characterization of lesions without the need for subsequent percutaneous biopsies.

References

  1. Ferrucci JT Jr., Wittenberg J, Mueller PR, et al. Diagnosis of abdominal malignancy by radiologic fine-needle aspiration biopsy. AJR 1980; 134:323 -330[Abstract]
  2. Gupta S, Madoff DC. Image-guided percutaneous needle biopsy in cancer diagnosis and staging. Tech Vasc Interv Radiol2007; 10:88 -101[Medline]
  3. Stewart CFT, Coldewey J, Stewart IS. Comparison of fine needle aspiration cytology and needle core biopsy in the diagnosis of radiologically detected abdominal lesions. J Clin Pathol2002; 55:93 -97[Abstract/Free Full Text]
  4. vanSonnenberg E, Lin AS, Casola G, Nakamoto SK, Wing VW, Cubberly DA. Removable hub needle system for coaxial biopsy of small and difficult lesions. Radiology 1984;152 : 226[Abstract/Free Full Text]
  5. Broderick LS, Kopecky KK, Cramer H. Image-guided coaxial fine needle aspiration biopsy with a side-exiting guide. J Comput Assist Tomogr 2002; 26:292 -297[CrossRef][Medline]
  6. vanSonnenberg E, Wittenberg J, Ferrucci JT Jr., Mueller PR, Simeone JF. Triangulation method for percutaneous needle guidance: the angled approach to upper abdominal masses. AJR 1981;137 : 757-761[Abstract/Free Full Text]
  7. Langen HJ, Close KC, Keulers P, et al. Artificial widening of the mediastinum to gain access for extrapleural biopsy: clinical results. Radiology 1995;196 : 703-706[Abstract/Free Full Text]
  8. Gupta S, Nguyen HL, Morello FA, et al. Various approaches for CT-guided percutaneous biopsy of deep pelvic lesions: anatomic and technical considerations. RadioGraphics 2004;24 : 763-786
  9. Akins EW, Hawkins IF Jr, Mladinich C, Tupler R, Siragusa RJ, Pry R. The blunt needle: a new percutaneous access device. AJR 1989; 152:181 -182[Free Full Text]
  10. Memel DS, Dodd GD, Esola CC. Efficacy of sonography as a guidance technique for biopsy of abdomen, pelvis, and retroperitoneal lymph nodes. Radiology 1997;205 : 185-190[Abstract/Free Full Text]
  11. Arrelano RS, Maher M, Gervais DA, Hahn PF, Mueller PR. The difficult biopsy: let's make it easier. Curr Probl Diagn Radiol 2003; 32:218 -226[Medline]
  12. Kinney TB, Lee MJ, Filomena CA, et al. Fine-needle biopsy: prospective comparison of aspiration versus nonaspiration techniques in the abdomen. Radiology 1993;186 : 549-552[Abstract/Free Full Text]
  13. Sze DY. Use of curved needles to perform biopsies and drainages of inaccessible targets. J Vasc Interv Radiol2001; 12:1441 -1444[Medline]
  14. Gupta S, Ahrar K, Morello FA Jr, Wallace MJ, Madoff DC, Hicks ME. Using a coaxial technique with a curved inner needle for CT-guided fine-needle aspiration biopsy. AJR 2002;179 : 109-112[Free Full Text]
  15. Lufkin RB, Gronemeyer DH, Seibel RM. Interventional MRI: update. Eur Radiol 1997;7 [suppl 5]:187 -200[Medline]
  16. Howard MH, Nelson RC, Paulson EK, et al. An electronic device for needle placement during sonographically guided percutaneous intervention. Radiology 2001;218 : 905-911[Abstract/Free Full Text]
  17. Bang N, Bachmann Nielsen M, Vejborg I, Mellon Mogensen A. Clinical report: contrast enhancement of tumor perfusion as a guidance for biopsy. Eur J Ultrasound 2000;12 : 159-161[CrossRef][Medline]
  18. Smith EH. Complications from percutaneous abdominal fine-needle biopsy. Radiology 1991;178 : 253-258[Abstract/Free Full Text]
  19. Brandt KR, Chaboneau JW, Stephens DH, et al. CT- and US-guided biopsy of the pancreas. Radiology 1993;187 : 99-104[Abstract/Free Full Text]
  20. Tung GA, Cronan JJ. Percutaneous biopsy of hepatic cavernous hemangioma. J Clin Gastroenterol 1993;16 : 117-122[Medline]
  21. Silverman SG, Gan YU, Morele KJ, Tuncali K, Cibas ES. Renal masses in the adult patient: the role of percutaneous biopsy. Radiology 2006;240 : 6-22[Abstract/Free Full Text]
  22. de Kerviler E, Guermazi A, Zagdanski AM, et al. Image-guided core-biopsy in patients with suspected or recurrent lymphomas. Cancer 2000; 89:649 -652

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