Comparison of Ultrasound-Guided Core Needle Biopsy and Endoscopic Ultrasound-Guided Fine-Needle Aspiration for Solid Pancreatic Lesions

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1 ORIGINAL RESEARCH Comparison of Ultrasound-Guided Core Needle Biopsy and Endoscopic Ultrasound-Guided Fine-Needle Aspiration for Solid Pancreatic Lesions Young Keun Sur, MD, Young Chul Kim, MD, Jai Keun Kim, MD, Jei Hee Lee, MD, Byung Moo Yoo, MD, Young Bae Kim, MD Received November 17, 2014, from the Departments of Radiology (Y.K.S., Y.C.K., J.K.K., J.H.L.), Gastroenterology (B.M.Y.), and Pathology (Y.B.K.), Ajou University School of Medicine, Suwon, Korea. Revision requested December 16, Revised manuscript accepted for publication March 6, Address correspondence to Young Chul Kim, MD, Department of Radiology, Ajou University School of Medicine, 164 World Cup-ro, Yeongtong-gu, Suwon , Gyeonggi-do, Korea. Abbreviations CNB, core needle biopsy; CT, computed tomography; EUS, endoscopic ultrasound; FNA, fine-needle aspiration; MRI, magnetic resonance imaging; US, ultrasound doi: /ultra Objectives The objective of our study was to compare the diagnostic yield of endoscopic ultrasound (EUS)-guided fine-needle aspiration (FNA) using a 25-gauge needle and ultrasound (US)-guided core needle biopsy (CNB) using an 18-gauge core needle for diagnosis of solid pancreatic lesions. Methods This retrospective study was approved by our Institutional Review Board, and the requirement for informed consent was waived. Patients who underwent either EUS-guided FNA or US-guided CNB for a solid pancreatic lesion from January 2008 to December 2012 were included and reviewed. Fine-needle aspirations and CNBs were performed by experienced endoscopists and radiologists. The diagnostic yield, accuracy, technical failure rate, sensitivity, and specificity for malignancy were calculated and compared. Results A total of 106 biopsy attempts were undertaken in 89 patients (EUS-guided FNA, n = 70; US-guided CNB, n = 36). Biopsy specimens were successfully obtained in 98 biopsy attempts (EUS-guided FNA, n = 63; US-guided CNB, n = 35). The accuracy, technical failure rate, sensitivity, and specificity of EUS-guided FNA for malignancy (73.02%, 10.00%, 77.78%, and 44.44%, respectively) was not significantly different from those of US-guided CNB (88.57%, 2.78%, 87.10%, and 100%, respectively; P.089). Diagnostic performance did not differ between the modalities according to the size and the location of the lesion in the pancreas. However, the diagnostic yield of US-guided CNB (86.11%) was higher than that of EUS-guided FNA (65.71%, P =.035). Conclusions The diagnostic yield of US-guided CNB for solid pancreatic lesions is superior to that of EUS-guided FNA. Key Words diagnostic yield; endoscopic ultrasound-guided fine-needle aspiration; gastrointestinal ultrasound; pancreatic malignancy; pancreatitis; ultrasound-guided core needle biopsy Commonly encountered solid pancreatic lesions in clinical practice include pancreatic adenocarcinomas, solid pseudo - papillary tumors, neuroendocrine tumors, and pancreatitis. Solid pancreatic lesions can be categorized as benign, borderline, and malignant lesions. Accurate diagnosis of lesions as benign or malignant should help clinicians establish proper treatment plans and avoid unnecessary surgery by the American Institute of Ultrasound in Medicine J Ultrasound Med 2015; 34:

2 Due to its high spatial resolution, endoscopic ultrasound (EUS) is useful for evaluation of pancreatic lesions. 1 Additionally, EUS-guided fine-needle aspiration (FNA) may provide cytologic assessment of solid pancreatic lesions. Endoscopic US-guided FNA using several different needles (25-, 22-, and 19-gauge TruCut needles) may be a less-invasive and effective technique for biopsy of solid pancreatic lesions. 2 In particular, the 25-gauge FNA needle is the best type of needle for acquisition of solid pancreatic lesions; the diagnostic accuracy and technical success rate are superior to those of 22- and 19-gauge needles. 3 Alternative modalities for biopsy of pancreatic lesions are percutaneous computed tomography (CT) and ultrasound (US)-guided core needle biopsy (CNB), which does not require an endoscopic procedure or sedation. Schoellnast et al 4 reported that the sensitivity of CT-guided percutaneous CNB was higher than that of FNA, although the difference did not reach statistical significance. Compared with CT-guided CNB, US-guided CNB is simpler and can avoid radiation exposure. Given that the diagnostic accuracy of US-guided CNB is comparable with that of EUS-guided FNA or CT-guided CNB, US-guided CNB would be a simple complementary procedure for histologic diagnosis of solid pancreatic lesions. To our knowledge, there have been no comparative studies concerning the diagnostic performance of USguided CNB and EUS-guided FNA of solid pancreatic lesions. The purpose of this study was to compare the diagnostic yield of US-guided CNB and EUS-guided FNA of solid pancreatic lesions. pancreatitis (n = 10). Distal pancreatectomy was performed in 7 patients, the Whipple procedure in 5, and pyloruspreserving pancreaticoduodenectomy in 7, liver biopsy in 16, and lung FNA in 3. Forty-two patients were inoperable because of major vessel invasion, including the celiac artery, superior mesenteric artery, superior mesenteric vein, and portal vein. Nine patients with pancreatitis had no interval change during follow-up of greater than 1 year, and 1 patient with pancreatitis underwent pylorus-preserving pancreaticoduodenectomy because of a false-positive pathologic report after EUS-guided FNA (Figure 1). Ultrasound-Guided CNB After each mass had been identified with CT, MRI, or US imaging, US-guided CNB was performed on request of a clinical department, usually the Department of Gastroenterology. There were no definite criteria for selection of the initial biopsy modality, and the decision was made by the clinician, who was also the endoscopist who performed EUS-guided FNA. Usually the clinician preferred EUS-guided FNA as the initial modality for biopsy; however, if the location of the lesion was considered unsuitable for EUS-guided FNA, or if pancreatitis was Figure 1. Flowchart of biopsy attempts and failures of both modalities. Materials and Methods Patient Population This retrospective study was approved by our Institutional Review Board, and the requirement for informed consent was waived. We included all patients who underwent EUSguided FNA, US-guided CNB, or both at our institution from January 2008 to December 2012 due to solid pancreatic lesions, which were detected on imaging modalities including CT and magnetic resonance imaging (MRI). The patients who met these inclusion criteria were identified by a computerized search of medical records. A total of 89 patients were identified and reviewed. Eighty-nine solid pancreatic lesions in 89 patients were confirmed either by surgery, liver biopsy, or lung biopsy of metastatic lesions or greater than 1 year of follow-up. The lesions included pancreatic adenocarcinoma (n = 74), adenosquamous carcinoma (n = 1), neuroendocrine tumors (n = 3), a solid pseudopapillary tumor (n = 1), and 2164 J Ultrasound Med 2015; 34:

3 suspected, the clinician would consider US-guided CNB as the initial biopsy modality. Also, in cases of inoperable cancer in which cancer seeding along the needle insertion track was not a concern, US-guided CNB was considered as the initial biopsy modality. Written consent was obtained from the patients for possible risks of the procedure, including bleeding and injury to adjacent organs. The patients fasted (both food and water) for at least 8 hours. The US-guided CNBs were all performed by experienced radiologists specializing in gastrointestinal radiology (J.K.K. and J.H.L., with 17 and 14 years of experience in abdominal imaging, respectively), who were aware of the lesion size and location from previous CT, MRI, or US imaging. One of 2 systems was used for the procedure: either an Acuson Sequoia 512 system (Siemens AG, Erlangen, Germany) with a 4-MHz curved probe or an iu22 xmatrix system (Philips Healthcare, Best, the Netherlands) with a 5-MHz curved probe. After the probe was pressed firmly against the abdominal wall, the needle insertion site was determined according to the location of the mass, and the shortest needle insertion route was selected to minimize the risk of injury to adjacent organs; color Doppler imaging was used to avoid vascular injury. Whenever possible, penetration of abdominal hollow viscera was avoided, and a trans peritoneal approach was preferred, but a transhepatic approach was also used in cases of pancreatic head lesions. If the transhepatic or transperitoneal approach was not possible, the biopsy attempt was aborted and counted as a technical failure. Local anesthesia with lidocaine was performed around the needle insertion site to minimize pain and facilitate patient cooperation without administration of any kind of sedative drugs. An 18-gauge core needle with a 22-mm throw length (Acecut; TSK Laboratory, Tochigi-shi, Japan) was percutaneously inserted under the assistance of a needle guidance system attached to the curved probe, and the course of needle insertion track was visualized on the screen of the US system. Biopsy samples were obtained at least twice according to the discretion of the radiologist. Samples were fixed in 10% formalin and sent to the Department of Pathology for histologic diagnosis. After US-guided CNB, the presence of immediate postprocedural complications was checked with US. Compression of the needle insertion site was done for 5 minutes to prevent hemorrhage, and the patient was sent back to the ward. The procedural process was briefly documented in the electronic medical record by the radiologist, including the character of the lesion and presence of complications. Endoscopic US-Guided FNA After written informed consent was obtained, 3 to 5 mg of midazolam was administrated intravenously with local pharyngeal anesthesia (2% lidocaine spray). Endoscopic US and FNA examinations were performed with a curved linear array channel endoscope (GF-UCT-2000; Olympus, Tokyo, Japan) with frequencies of 5, 7.5, and 12 MHz and a miniprobe (Olympus) with a frequency of 20 MHz. A deaerated water-filled balloon was attached around the tip of the transducer to allow the US beam to penetrate without interference from the intraluminal air component. A 25-gauge needle with a side port that enabled aspiration from the needle s distal tip and side was used. The needle was passed at least twice according to the discretion of the endoscopist. All EUS and EUS-guided FNA examinations were performed by experienced endoscopists (with 16 and 12 years of experience2164) who were aware of the size and location of the lesions detected on previous CT, MRI, or US imaging. Statistical Analyses Statistical analyses were performed with commercial software (SPSS version 20; IBM Corporation, Armonk, NY). Differences in patient age, sex, final diagnosis, lesion size, and location were analyzed by an independent ttest. P<.05 was considered statistically significant. The technical failure rate, sensitivity, diagnostic accuracy, and yield of EUS-guided FNA and US-guided CNB were compared by a generalized estimating equation approach, since some patients underwent repeated biopsy with the other modality. Specificity was compared by the Fisher exact test because there were only a few cases (n = 13) of benign lesions. Technical failure was defined as failure to obtain a biopsy specimen due to approach failure. 3 Sensitivity, specificity, and accuracy were calculated among cases in which biopsy specimens were obtained. 5 Diagnostic yield was defined as the proportion of accurate diagnoses among all cases, including the cases with technical failure. 6 The diagnostic yield and accuracy of the modalities according to lesion size were compared by the Fisher exact test after categorizing the lesions into 3 different size groups: smaller than 2 cm, 2 to 4 cm, and larger than 4 cm. In addition, the diagnostic yield of each modality according to lesion location was calculated and compared after grouping pancreatic head and uncinate lesions in the same category, pancreatic neck and body lesions in the same category, and pancreatic tail lesions in as a separate category. The pancreatic neck was defined as the portion of the pancreas ventrally overlying the superior mesenteric vein, and the border between the pancreatic body and tail was defined as half the distance between the neck and end of the pancreas. 7 J Ultrasound Med 2015; 34:

4 Results The 89 patients included 49 men and 40 women with a mean age of years (range, years). Patient characteristics and the diagnostic performance of each modality are summarized in Table 1. There were no complications in all EUS-guided FNAs and US-guided CNBs that could be classified as major complications according to the classification published by the Society of Vascular and Interventional Radiology. 8 Minor complications were present in 3 of 70 patients (4.3%) after EUS-guided FNA and 6 of 36 patients (16.7%) after US-guided CNB. Two patients had transient abdominal pain, and 1 patient had transient fever after EUS-guided FNA. All 6 cases of minor complications after US-guided CNB were transient abdominal pain, which subsided within 24 hours. The mean ages of patients who underwent EUS-guided FNA and US-guided CNB were years (range, years) and years (range, years), respectively, without a significant difference (P =.720). The sizes of the lesions on each modality ranged from 1 to 8 cm for EUSguided FNA and 1 to 6.9 cm for US-guided CNB, with mean values of 3.52 and 3.66 cm, respectively. There was no significant difference in lesion size between the modalities (P =.543). A total of 106 biopsy attempts (EUS-guided FNA, n = 70; US-guided CNB, n = 36) were undertaken in 89 patients, and biopsy specimens were successfully obtained in 98 biopsy attempts (EUS-guided FNA, n = 63; US-guided Table 1. Characteristics of Patients Who Initially Underwent EUS- Guided FNA and US-Guided CNB for Solid Pancreatic Lesions FNA CNB Characteristic (n = 70) (n = 36) P Malignancy 61 (87.14) 32 (88.89).958 Adenocarcinoma Adenosquamous carcinoma 1 0 Neuroendocrine tumor 3 2 Solid pseudopapillary tumor 1 0 Pancreatitis 9 4 Age, mean ± SD ± ± Sex 35 (50.00) 25 (69.44).088 Male 35 (50.00) 11 (30.56) Female Size, cm 3.52 ± Location.312 Head and uncinate 40 (57.14) 26 (72.22) Body and neck 19 (27.14) 6 (16.67) Tail 11 (15.72) 4 (11.11) Data are presented as mean ± SD, number of patients, and number of patients (percent). CNB, n = 35; Figure 1). Biopsy specimens were successfully obtained from 63 of 70 patients who underwent EUSguided FNA attempts. Biopsy attempts using US-guided CNB were successful in 35 of 36 patients. Biopsy attempts were undertaken with both modalities in 17 patients because of technical failure of the initial attempt (n = 7) and presumed inaccurate diagnoses (n = 10). The 10 patients with initial presumed inaccurate diagnoses underwent repeated biopsy attempts with the other modality, even though biopsy specimens were successfully obtained in the initial biopsy attempts. There was no statistically significant difference in the technical failure rate between EUS-guided FNA (7 of 70 [10.00%]) and US-guided CNB (1 of 36 [2.78%]; P=.158). In every case of technical failure, biopsy was attempted using the other modality. In 6 patients, initial biopsy attempts with EUS-guided FNA were unsuccessful, but subsequent attempts with US-guided CNB were successful. In 1 other patient, biopsy attempts were unsuccessful with both modalities. Those 7 patients who had been switched to the other modality due to initial technical failure were confirmed as having pancreatic adenocarcinoma (n = 6) and a neuroendocrine tumor (n = 1) on pathologic evaluation. The lesion locations in cases with technical failure of EUS-guided FNA were the pancreatic head (n = 1), uncinate (n = 3), body (n = 1), and tail (n = 1; Figure 2). In the case with technical failure of both modalities, the lesion was located in the pancreatic tail (n = 1). Among 70 patients who underwent EUS-guided FNA, pancreatic adenocarcinoma (n = 56), adenosquamous carcinoma (n = 1), neuroendocrine tumors (n = 3), a solid pseudopapillary tumor (n = 1), and pancreatitis (n = 9) were finally diagnosed. The final diagnoses in 36 patients who underwent US-guided CNB were pancreatic adenocarcinoma (n = 30), neuroendocrine tumors (n = 2), and pancreatitis (n = 4). A correct histologic diagnosis by EUS-guided FNA was made in 42 of 54 malignancies (sensitivity, 77.78%) and 4 of 9 benign pancreatitis lesions (specificity, 44.44%). One of 9 patients with pancreatitis underwent pylorus-preserving pancreaticoduodenectomy because of a false-positive pathologic report after EUS-guided FNA (Figure 3). Diagnoses of 8 cases of pancreatitis were verified by USguided CNB (n = 3) or clinical and imaging follow-up of greater than 1 year (n = 5). The diagnostic accuracy for solid pancreatic lesions on EUS-guided FNA was 73.02% (46 of 63). A correct diagnosis by US-guided CNB was made in 27 of 31 malignancies (sensitivity, 87.10%) and 4 of 4 benign pancreatitis lesions (specificity, 100%). The diagnostic accuracy for solid pancreatic lesions on US J Ultrasound Med 2015; 34:

5 Figure 2. Images from a 51-year-old male patient who underwent pylorus-preserving pancreaticoduodenectomy after EUS-guided FNA. A. An approximately 2.4-cm slightly hypoenhancing lesion (arrow) with peripancreatic fatty infiltration was noted in the pancreatic uncinate process. B, On an endoscopic US examination, a cm well-demarcated hypoechoic masslike lesion (arrow) was seen in the pancreatic uncinate process. The histologic diagnosis using EUS-guided FNA was malignancy, but the case was later confirmed as benign pancreatitis after surgical resection (pancreas-preserving pancreaticoduodenectomy). Figure 3. Images from a 69-year-old male patient with pancreatic tail cancer who underwent US-guided CNB. A, A 3.8-cm hypoattenuating mass (arrow) was seen in the pancreatic tail with suspected invasion to the splenic hilum. An initial EUS-guided FNA attempt failed to approach the lesion, and the patient was referred for US-guided CNB. B, On a percutaneous sonogram, a poorly defined hypoechoic mass was seen in the pancreatic tail near the splenic hilum. The core needle was inserted through the anterior abdominal wall parallel to the medial border of spleen. The case was confirmed as adenocarcinoma. C, A color Doppler examination was performed to avoid vascular injury during biopsy. There were no vessels in the course of the needle insertion track or adjacent to the lesion. J Ultrasound Med 2015; 34:

6 guided CNB was 88.57% (31 of 35). The differences in sensitivity (P =.303), specificity (P =.105), and diagnostic accuracy (P =.089) between EUS-guided FNA and USguided CNB did not reach statistical significance. The diagnostic yield and diagnostic accuracy of each modality were not significantly different in the 3 lesion-size groups, although the results were superior for US-guided CNB. Both the diagnostic yield and accuracy increased for both modalities in the groups of larger lesions (Table 2). The diagnostic yield of each modality according to lesion location did not show a significant difference between EUS-guided FNA and US-guided CNB (head and uncinate, 60.00% versus 84.62; P =.054; body and neck, 78.95% versus 100%; P =.540); tail, 63.64% versus 75%; P =.999). However, the overall diagnostic yields of EUSguided FNA and US-guided CNB were 65.71% (46 of 70) and 86.11% (31 of 36), respectively, with a statistically significant difference (P =.035). Discussion The histopathologic result for a solid pancreatic lesions as benign or malignant affects the diagnostic workup and planning. An accurate diagnosis is influenced by the lesion size, location, needle gauge, and presence or absence of pancreatitis Greater accuracy of percutaneous biopsy was reported for larger solid pancreatic lesions (>3.0 cm, 92%; 3 cm, 81%). 11 In another report, tumor size did not influence the ability to obtain informative biopsy samples if the lesion was larger than 2.5 cm. 12 In our study, the average lesion size was not significantly different between patients who underwent EUS-guided FNA (3.52 cm) and US-guided CNB (3.66 cm). In addition, there were no significant differences in diagnostic performance between the modalities after we divided the lesions into 3 different size groups (Table 2). A previous meta-analysis of EUS-guided FNA demonstrated that 25-gauge needles are more sensitive than 22-gauge needles for diagnosing pancreatic malignancy (93% versus 85%; P =.0003). 9 We compared the diagnostic performance of US-guided CNB and EUS-guided FNA using a 25-gauge needle, as in other previous studies. Thus, the lesion size and needle gauge might not have affected our study comparing the diagnostic performance of both modalities. The sensitivity of US-guided CNB has been reported to be 71% to 99% Previously estimated sensitivity and specificity of EUS-guided FNA (75% 92% and 82% 100%, respectively) are comparable to the values in our study. Sensitivity values of EUS-guided FNA and US-guided CNB are reportedly lower in patients with chronic pancreatitis than in those without chronic pancreatitis. 10,15 Our study enrolled 10 patients with pancreatitis, which might have affected the sensitivity of both modalities. In our study, the sensitivity, specificity, and accuracy of US-guided CNB (87.10%, 100%, and 88.57%, respectively) were comparable to those of EUS-guided FNA (77.78%, 44.44%, and 73.02%). The diagnostic performance of the biopsy modality could be associated with the lesion location. It has been reported that the diagnostic accuracy of percutaneous CT- or US-guided biopsy for lesions located in the body or tail of the pancreas (93%) is higher than for lesions located in the pancreatic head (84%). 11 Although it was not statistically significant, the lowest P value (.054) was observed for the diagnostic yields of pancreatic head and uncinate lesions, which were 60.00% for EUS-guided FNA and 84.62% for US-guided CNB. The diagnostic yield according to lesion location was not significantly different between the modalities. However, the overall diagnostic yield was significantly higher for US-guided CNB (86.11%) than EUS-guided FNA (65.71%; P =.035). Diagnostic yields according to lesion location were superior for US-guided CNB but without statistical significance. In addition, the technical failure rate for EUS-guided FNA was higher than that for US-FNA, without statistical significance. These findings might have contributed to the statistically significant difference in the diagnostic yield between the modalities. We can assume that US-guided CNB could be used as an alternative or complementary procedure in place of or in addition to EUSguided FNA. Although there were no major procedure-related complications in our study, caution should be used for possible complications after percutaneous biopsy. Table 2. Comparison of Diagnostic Yield and Diagnostic Accuracy Between EUS-Guided FNA and US-Guided CNB According to Pancreatic Lesion Size FNA CNB Characteristic (n = 70) (n = 36) P Diagnostic yield <2 cm 5/12 (41.67) 3/4 (75.00) cm 23/34 (67.65) 16/19 (84.21).330 >4 cm 18/24 (75.0) 12/13 (92.3).383 Diagnostic accuracy <2 cm 5/11 (45.46) 3/4 (75.00) cm 23/28 (82.14) 16/18 (88.89).688 >4 cm 18/24 (75.00) 12/13 (92.30).383 Data are presented as number of patients (percent) J Ultrasound Med 2015; 34:

7 Hemorrhage, acute pancreatitis, pancreatic fistulas, abscesses, intraperitoneal seeding of malignant pancreatic tumors, and even death may occur in patients after CT- or USguided CNB of the pancreas, although the actual reported complication rate is low. 16,17 In a series by Tillou et al, 17 the complication rate for percutaneous FNA biopsy of the pancreas was 3.4%. In their series, 3 cases of major complications developed after percutaneous FNA biopsy of pancreas, with 1 fatal case of procedure-related necrotizing pancreatitis. Similarly, Mueller et al 16 reported 5 cases of severe pancreatitis after percutaneous biopsy in a series of 184 patients. This study had several limitations. Above all, there were few patients with pancreatitis (10 of 89 [11.24%]). A total of 106 biopsy attempts in 89 patients were included. With a larger target population, some results might have shown statistical significance. Further prospective research with a larger population of patients with pancreatitis might be needed to evaluate the statistical significance of the technical failure rate and diagnostic performance between the modalities. The lack of surgical confirmation of diagnoses was another limitation of this study. Forty-two cases were inoperable malignancy cases, and 8 were benign pancreatitis cases, which should not be treated surgically. However, the possibility of an incorrect final diagnosis would have been very low because all patients without surgical confirmation underwent at least 1 year of CT follow-up unless the patient died of malignancy. Especially, inoperable malignant cases displayed obvious malignant features on CT or MRI with concordant changes during follow-up. In cases of pancreatitis, we think that 1 year of follow-up would suffice for a benign diagnosis. Finally, the possibility of interoperator differences was another limitation of this study. Endoscopic USguided FNAs and US-guided CNBs were performed by 2 different endoscopists and radiologists, and it is possible that the difference in technical skill of each operator might have influenced the results. However, considering that each operator had many years of experience in gastroenterology or radiology (endoscopists, 16 and 12 years of experience; radiologists, 17 and 14 years of experience), variations in technical skill among operators was anticipated to have been insignificant. Also, in cases of technical difficulty, the more experienced operator was asked for supervision and consensus. In conclusion, the diagnostic performance of USguided CNB was superior to that of EUS-guided FNA for assessment of solid pancreatic lesions. Ultrasound-guided CNB might be complementary to EUS-guided FNA for accurate diagnosis of solid pancreatic lesions. References 1. Kim YC, Choi JY, Chung YE, et al. 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