CT-Guided Biopsy of Perivascular Tumor Encasement Using Simultaneous IV Contrast Enhancement

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1 Vascular and Interventional Radiology Clinical Observations Collins et al. CT-Guided iopsy of Perivascular Tumor Vascular and Interventional Radiology Clinical Observations FOCUS ON: Joseph M. Collins 1 J. Scott Kriegshauser 1 Kevin O. Leslie 2 Collins JM, Kriegshauser JS, Leslie KO Keywords: biopsy, CT, ductal adenocarcinoma pancreas, metastasis, needle, neoplasm, pancreatic neoplasms DOI: /JR Received October 13, 2008; accepted after revision January 31, Department of Radiology, Mayo Clinic, E Shea lvd., Scottsdale, Z ddress correspondence to J. M. Collins (collins.joseph@mayo.edu). 2 Division of natomic Pathology, Mayo Clinic, Scottsdale, Z. WE This is a Web exclusive article. JR 2009; 193:W283 W X/09/1934 W283 merican Roentgen Ray Society CT-Guided iopsy of Perivascular Tumor Encasement Using Simultaneous IV Contrast Enhancement OJECTIVE. The purpose of our study was to describe and review the accuracy of a novel technique for difficult biopsy of arterial tumor encasement using simultaneous IV contrast enhancement and helical CT guidance for coaxial core needle biopsies. CONCLUSION. Diagnostic biopsy specimens can be obtained safely using simultaneous IV contrast-enhanced CT guidance during difficult biopsies of unresectable tumors encasing the celiac, superior mesenteric, or renal arteries. P erivascular tumor encasement, often found in patients with ductal adenocarcinoma of the pancreas, is a sign of unresectability [1]. Most patients have other more easily targeted sites of tumor involvement that allow biopsy using endoscopic ultrasound (EUS), transabdominal ultrasound, or routine biopsy guided by helical CT. However, when other biopsy techniques are not possible or have proven to be unsuccessful, direct biopsy of the encasing perivascular soft tissue becomes important. We describe a novel technique using simultaneous IV contrast enhancement and CT guidance to accurately and safely sample tumor encasement of arteries and veins. Materials and Methods We retrospectively reviewed 11 consecutive patients who underwent CT-guided contrast-enhanced biopsy of perivascular tumor encasement between 2004 and 2008 at our tertiary care academic medical center from among 1,385 CTguided and 9,576 ultrasound-guided biopsies performed here during that period. Ten were men between the ages of 44 and 85 years; the age of the one woman was 61 years (Table 1). posterior paraspinal approach was used in 10 patients (nine and one right). In one patient (patient 10), an anterior approach was used. First, a guide needle was placed using CT fluoroscopic guidance without IV contrast enhancement. focal calcified arterial plaque sometimes served as a useful landmark to help position the guide needle as close as possible to the desired biopsy track. Next, with the guide needle in place, IV contrast-enhanced CT was performed with late arteri- al phase timing (43 seconds). These examinations were performed on a 16-MDCT scanner (Somatom Sensation 16, Siemens Healthcare), with kvp of 140 and quality reference ms of 240. The use of contrast material ranged from 50 to 150 ml of one of the following: iohexol 300 mg I/mL, iohexol 350 mg I/mL, or iodixanol 320 mg I/mL (Table 1). Injection rates were 3 4 ml/s. The CT images depicted the relation of the needle to the important nearby vascular structures, and the rind of perivascular tumor encasement that was the target of the biopsy (Fig. 1). The 3D axial, coronal, and sagittal oblique images precisely showed the relation of the biopsy track to the peripancreatic arteries. sagittal oblique reformatted image showed the full length of the guide needle (Figs. 2 and 3). On coronal reformatted images, the hypodense metallic streak artifact from the tip of the guide needle indicated the biopsy track extending into the rind of the perivascular tumor encasement (Fig. 3). Using these reformatted images, we could make precise final adjustments before proceeding with the biopsy. Once the guide needle was at the desired angle to the target, 4 8 coaxial biopsies were performed. With a manually advanced, spring-loaded automatic coaxial biopsy needle system, the position of the exposed cutting chamber within the perivascular mass could be verified with CT fluoroscopy before the core biopsy specimen was actually obtained (Fig. 1). The biopsy needle was rotated to face the cutting chamber away from the adjacent artery (Fig. 2). In most cases, a 19-gauge guide needle was used, but in one case each, a 17-gauge and a 20- gauge needle were used. Coaxial 20-gauge Temno biopsy needles (llegiance Health Care) were used JR:193, October 2009 W283

2 Collins et al. TLE 1: Characteristics of 11 Consecutive Patients Who Underwent CT-Guided iopsy of Perivascular Tumors Patient No. Sex ge (y) Encased Vessel Prior Nondiagnostic iopsy most often in this series; other biopsy needles included 20-gauge automated spring-loaded biopsy needles (Easy Core iopsy System, oston Scientific) and 20- and 22-gauge manual-cutting biopsy needles (Sure-Cut, oston Scientific). The size and type of needle were determined by the radiologist on the basis of the difficulty of the target (Table 1). s we gained experience, we favored the Temno needle. We usually prepared a slurry of Surgifoam bsorbable Gelatin Sponge (Ferrosan, distributed by Ethicon) in a 1-mL tuberculin syringe for injection into the guide needle to suppress any back bleeding observed through the guide needle. This study was HIP-compliant, and the institutional review board screened and approved the retrospective review of patient records of persons who underwent biopsy using simultaneous IV contrast enhancement with CT guidance. Results This technique resulted in a positive diagnosis of malignancy in all 11 patients. There were no bleeding complications. In one case Diagnosis fter iopsy a 1 M 44 SM ERCP brush C pancreas or biliary 2 M 65 SM CT, EUS, ERCP brush, surgery Cancer ntigen 19 9 (U/mL) b iopsy pproach 88 Posterior C pancreas 274 Posterior 3 M 69 C EUS C pancreas 118 Posterior 4 M 74 C CT C pancreas 1,728 Posterior right 5 M 63 C and SM 6 M 73 SM and PV EUS, CT aborted C pancreas < 1 Posterior EUS C pancreas 1,431 Posterior 7 M 72 C EUS C pancreas 2,632 Posterior 8 M 81 C and SM None C pancreas < 1 Posterior 9 M 85 Left R CT Metastatic prostate adenocarcinoma 10 F 61 SMV and PV ERCP brush, CT aborted N Posterior Guide and Coaxial Needle Gauge (patient 7), there was slight oozing from the guide needle, without significant hemorrhage, that was suppressed by injecting a Surgifoam slurry. The use of the Surgifoam slurry was not necessary in the other 10 patients. Eight of the 11 patients had high-grade ductal adenocarcinoma metastasized from the pancreas (Table 1). One patient (patient 1) had a high-grade adenocarcinoma from an unknown primary source encasing the superior mesenteric artery (SM). One patient (patient 9) with a solitary functioning kidney had metastatic prostate adenocarcinoma encasing the renal artery. One patient (patient 11) had high-grade, poorly differentiated, transitional carcinoma encasing the renal artery. Ten of the 11 patients had undergone one or more previously unsuccessful CT-guided, ERCP brush, EUS-guided, or surgical nondiagnostic biopsies (Table 1). Two of the 11 had been referred for a routine CT-guided biopsy that was aborted because the radiologist believed a biopsy would be too risky. No. of Passes Type of Needle Contrast Material Iodine IV Contrast Concentration Material (ml) (mg I/mL) 17/19 and 21 7 Sure-Cut c Iohexol /20 8 Temno d Iodixanol /20 4 Temno d Iohexol /20 6 SP e and Temno d Iohexol /20 4 Temno d Iodixanol /20 5 SP e Iohexol /20 5 Temno d Iohexol /22 6 Temno d Iodixanol /20 6 SP e and Temno d Iodixanol C pancreas 15,462 nterior 19/20 6 Temno d Iohexol M 75 Left R CT Metastatic TCC N Posterior 19/20 5 Temno d Iohexol Note SM = superior mesenteric artery, C = celiac artery, PV = portal vein, R = renal artery, SMV = superior mesenteric vein, EUS = endoscopic ultrasound, C = adenocarcinoma, TCC = transitional cell carcinoma, N = not available. a Using IV contrast technique. b Normal cancer antigen 19 9 is < 40 U/mL. c Manufactured by oston Scientific. d Manufactured by llegiance Health Care. e Manufactured by Microvasive. In a particularly difficult case (patient 2), nondiagnostic attempts at routine CT-guided biopsy and EUS biopsy and repeated unsuccessful attempts at endoscopic biopsy eventually led to open surgery for biopsy. ll the biopsy attempts proved negative for malignancy. The perivascular soft-tissue rind on CT remained worrisome for invasive pancreatic carcinoma, but 13 months elapsed before treatment could be initiated with chemoradiotherapy after a positive biopsy specimen was obtained using our technique (Fig. 3). One patient (patient 8) had previously undergone a total pancreatectomy for grade 3 invasive ductal adenocarcinoma, followed by postoperative external-beam radiotherapy and chemotherapy. Slowly progressive softtissue thickening developed between the celiac artery and the SM, mimicking the appearance of postoperative and postradiation fibrosis. biopsy specimen using our technique showed recurrent adenocarcinoma. One patient (patient 9) had undergone a previous nondiagnostic CT-guided aspiration W284 JR:193, October 2009

3 CT-Guided iopsy of Perivascular Tumor from tissue encasing the renal artery. This patient had a solitary functioning kidney, so it was particularly important to avoid injury of the renal artery. Using our technique, we obtained core biopsy specimens from an area 3 mm superior to the renal artery (Fig. 4). lthough lymphoma had initially been suspected on CT, these biopsy specimens confirmed metastatic adenocarcinoma from the prostate. Fig year-old man (patient 5) who underwent posterior paraspinal biopsy with simultaneous IV contrast enhancement., xial CT image obtained during procedure shows streak artifact from guide needle tip pointing to 5-mm rind of tumor encasing superior mesenteric artery (SM)., xial CT image shows cutting chamber of coaxial biopsy needle deployed within rind of tumor encasing SM. Discussion Celiac and SM encasement is a hallmark of unresectable tumor spread of ductal adenocarcinoma of the pancreas [2, 3]. In some cases, this perivascular encasement is the only sign of unresectability. Occasionally, this perivascular encasement is the only suspicious finding. In such cases, it is important to be able to safely and effectively biopsy the encasing tumor so that appropriate treatment can be initiated. Perivascular encasement also occurs at other sites, such as the renal artery in patients 9 and 11 in this series. For many years, patients with ductal adenocarcinoma of the pancreas had poor long-term survival after surgical resection, although a subset of patients without extrapancreatic tumor spread at surgery had a somewhat better survival [4]. The combination of new protocols of preoperative chemoradiation with advances in surgical technique has led to new treatment approaches for locally advanced pancreatic carcinoma [5]. Segmental vascular resection offers additional treatment opportunities for patients at the cusp of surgical resectability. Candidates for complete margin negative (R0) surgical resection include patients with tumor encasement of a short segment of the hepatic artery that spares the celiac artery, involvement of less than half the circumference of Fig year-old man (patient 7) who underwent posterior paraspinal biopsy with simultaneous IV contrast enhancement., Parasagittal reformatted CT image obtained during biopsy. Note location of celiac artery adjacent to needle tip. Streak artifact from needle tip shows biopsy track that points to 3-mm rind of tumor along inferior surface of celiac artery., CT image shows biopsy needle deployed within rind of tumor along inferior surface of celiac artery. Cutting chamber is rotated away from artery to avoid bleeding complication. JR:193, October 2009 W285

4 Collins et al. Fig year-old man (patient 2) who underwent biopsy. SM indicates superior mesenteric artery., Parasagittal reformatted CT image aligned with plane of biopsy needle during simultaneous IV contrast enhancement depicts complex anatomy of biopsy track and adjacent arteries. Guide needle passes safely above renal artery. Streak artifact from needle tip points to invasive tumor inferior in relation to splenic artery., In this coronal reformatted CT image, streak artifact from needle tip is nestled between celiac, superior mesenteric, and splenic arteries and within retropancreatic tumor spread. External biliary stent extends to third portion of duodenum. the SM, or segmental occlusion of the confluence of the superior mesenteric and portal veins [6]. technique for safely and effectively biopsying the narrow cuff of tumor that encases the celiac artery or the SM and its branches can be crucial to the proper identification of those patients who are just beyond the bounds of surgical resectability. EUS-guided fine needle aspiration biopsy is useful for diagnosis of pancreatic malignancy, with an accuracy rate as high as 92% [7]. However, despite best efforts with EUS, brush cytology during ERCP [8, 9], percutaneous ultrasound-guided biopsy, or routine CT-guided biopsy (without simultaneous IV contrast enhancement), it can sometimes be difficult to establish proof of malignancy. To avoid subjecting a patient with benign disease to the morbidity, risk, and expense of unnecessary therapy, biopsy proof is generally required before initiating chemoradiotherapy. Pancreatic carcinoma often incites an exuberant fibroinflammatory response [10]. The number of anaplastic cells in a biopsy specimen is often rather sparse (Fig. 5). s a result, false-negative results of biopsies may occur with small-gauge aspiration needles. Therefore, when it is safe to do so, we prefer to use cutting needles to obtain cores of tissue suitable for histologic examination. To avoid sampling error and to reduce the likelihood of false-negative findings, we use a coaxial approach to obtain multiple biopsy specimens through the same guide needle. In our study, as many as eight biopsies were obtained; we stopped when we determined that we had obtained sufficient material for the pathologist. The use of a guide needle also allowed us to retain access for administering a Surgifoam slurry, if necessary. To avoid bleeding complications while using cutting needles to biopsy the thin rind of Fig year-old man (patient 9) who underwent biopsy., xial CT image obtained during simultaneous IV enhancement shows needle tip in tumor encasing renal artery supplying solitary functioning kidney. Note atrophic right kidney., Sagittal oblique reformatted CT image better depicts relation of guide needle tip to lumen of renal artery. W286 JR:193, October 2009

5 CT-Guided iopsy of Perivascular Tumor Fig year-old man (patient 7) who underwent posterior paraspinal biopsy with simultaneous IV contrast enhancement. Photomicrograph with high-power inset shows malignant gland within background of scirrhous fibroinflammatory tissue. Number of anaplastic cells is sparse within biopsy specimen. Two other full-chamber core biopsy specimens showed only exuberant fibroinflammatory response but no malignant cells. These findings show the value of repeat coaxial biopsies to avoid sampling error. (H and E, original magnification 200 and 400 [inset]). tumor that encased the peripancreatic arteries, we had to be very careful about the placement of the biopsy needle. However, the vascular road map provided by a previous IV contrastenhanced CT scan may be of little value at the time of biopsy, when the biopsy is guided only by unenhanced CT fluoroscopy. The tumor mass, the adjacent arteries and veins, and nearby collapsed loops of bowel all have a similar solid density on unenhanced CT. If the tumor mass encasing the artery cannot be safely distinguished from the artery itself on an unenhanced examination, then the radiologist using standard techniques may choose to not attempt the biopsy. We preferred to use the posterior approach because it made the needle and the target less prone to breathing motion and avoided the bowel. posterior paraspinal approach with a shallow angle of obliquity allowed the guide needle to pass safely by the side of the aorta to reach the side of the celiac artery, the central portion of the splenic artery, the central portion of the gastric artery, the side of the SM, or the renal artery. Care was taken to avoid traversing these arteries as well as the renal vein. right posterior paraspinal approach is more challenging but still can be done safely. In this approach, the guide needle must pass through the narrow slot between the inferior vena cava and the aorta to reach the right side of the celiac artery, the SM, and their branches. transcaval approach can be useful for fine-needle aspiration of pancreatic masses with a 22-gauge needle [11]. However, in our patients, we needed multiple cores with a cutting needle to overcome the sampling error often found with these desmoplastic tumors, so we did not use the transcaval approach. These findings are limited by the retrospective nature of our study and the small number of patients (n = 11) who underwent this novel biopsy procedure. lthough we successfully diagnosed malignancy in 100% of the patients, it was a small series. enign perivascular soft tissue is rare but has been reported with chronic pancreatitis [12]. In conclusion, we used helical CT with simultaneous IV contrast enhancement and multiplanar reformatting to safely and successfully obtain core needle biopsy specimens from perivascular tumor encasement. The technique allowed precise needle biopsy within a few millimeters of the arterial lumen. It was especially useful in patients whose ductal adenocarcinoma of the pancreas had proven resistant to diagnosis with other biopsy techniques. References 1. Katz MH, Hwang R, Fleming J, Evans D. Tumor-node-metastasis staging of pancreatic adenocarcinoma. C Cancer J Clin 2008; 58: Lu DS, Reber H, Krasny RM, Kadell M, Sayre J. Local staging of pancreatic cancer: criteria for unresectability of major vessels as revealed by pancreatic-phase, thin-section helical CT. JR 1997; 168: Hawes RH, Xiong Q, Waxman I, Chang KJ, Evans D, bbruzzese JL. multispecialty approach to the diagnosis and management of pancreatic cancer. m J Gastroenterol 2000; 95: Nitecki SS, Sarr MG, Colby TV, van Heerden J. Long-term survival after resection for ductal adenocarcinoma of the pancreas: is it really improving? nn Surg 1995; 221: Lall CG, Howard TJ, Skandarajah, DeWitt JM, isen M, Sandrasegaran K. New concepts in staging and treatment of locally advanced pancreatic head cancer. JR 2007; 189: Talamonti M. orderline resectable pancreatic cancer: a new classification for an old challenge. nn Surg Oncol 2006; 13: Raut CP, Grau M, Staerkel G, et al. Diagnostic accuracy of endoscopic ultrasound-guided fine-needle aspiration in patients with presumed pancreatic cancer. J Gastrointest Surg 2003; 7: Lee JG, Leung J. Tissue sampling at ERCP in suspected pancreatic cancer. Gastrointest Endosc Clin N m 1998; 8: Lee JG. rush cytology and the diagnosis of pancreaticobiliary malignancy during ERCP. Gastrointest Endosc 2006; 63: Cubilla, Fitzgerald PJ. Pancreas cancer. I. Duct adenocarcinoma: a clinical pathologic study of 380 patients. Pathol nnu 1978; 13: Gupta S, hrar K, Morello F Jr, Wallace MJ, Hicks ME. Masses in or around the pancreatic head: CT-guided coaxial fine-needle aspiration biopsy with a posterior transcaval approach. Radiology 2002; 222: Luetmer PH, Stephens DH, Fischer P. Obliteration of periarterial retropancreatic fat on CT in pancreatitis: an exception to the rule. JR 1989; 153:63 64 JR:193, October 2009 W287