Histologic diagnosis of pancreatic masses using 25-gauge endoscopic ultrasound needles with and without a core trap: a multicenter randomized trial
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1 632 Histologic diagnosis of pancreatic masses using 25-gauge endoscopic ultrasound needles with and without a core trap: a multicenter randomized trial Authors Ken Kamata 1, Masayuki Kitano 1, Satoru Yasukawa 2, Masatoshi Kudo 1, Yasutaka Chiba 3, Takeshi Ogura 4, Kazuhide Higuchi 4, Nobuyasu Fukutake 5, Reiko Ashida 5, Tomoaki Yamasaki 6, Hiroko Nebiki 6, Satoru Hirose 7, Noriyuki Hoki 7, Masanori Asada 8, Shujiro Yazumi 8, Makoto Takaoka 9, Kazuichi Okazaki 9, Fumihiro Matsuda 10, Yoshihiro Okabe 10, Akio Yanagisawa 2 Institutions Institutions are listed at end of article. submitted 8. May 2015 accepted after revision 23. February 2016 Bibliography DOI /s Published online: Endoscopy 2016; 48: Georg Thieme Verlag KG Stuttgart New York ISSN X Corresponding author Masayuki Kitano, MD Department of Gastroenterology and Hepatology Kinki University School of Medicine Ohno-higashi Osaka-sayama Japan m-kitano@med.kindai.ac.jp Background and study aims: Endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) with 25-gauge needles yields small volume samples that are mainly processed for cytology. Using 25-gauge needles with a core trap may overcome this limitation. This trial compared 25-gauge needles with and without a core trap in terms of their ability to obtain histologic samples from solid pancreatic masses. Patients and methods: Consecutive patients with solid pancreatic masses who presented to eight Japanese referral centers for EUS-FNA in April September 2013 were randomized to undergo sampling with a 25-gauge needle with a core trap (ProCore) or a standard 25-gauge needle. Tissue samples were fixed in formalin and processed for histologic evaluation. For the purpose of this study only samples obtained with the first needle pass were used for comparison of: (i) accuracy for the diagnosis of malignancy, (ii) rate of samples Introduction Endoscopic ultrasound (EUS)-guided fine needle aspiration (FNA) was developed for the pathologic diagnosis of lesions in and adjacent to the digestive tract [1]. In the setting of solid pancreatic masses, EUS-FNA has a diagnostic sensitivity of 54 % 96 %, a specificity of 96 % 98 %, and an accuracy of 83 % 95 % [2 5]. Several studies have shown that compared to 22- gauge and 19-gauge needles, 25-gauge needles are more maneuverable (particularly when difficult regions have to be accessed), can penetrate the mass more easily, and are less likely to yield samples contaminated with blood [6 9]. Moreover, a recently published meta-analysis showed that a 25-gauge FNA needle was more sensitive than a 22-gauge FNA needle for diagnosing solid pancreatic tumors (pooled sensitivity, 93 % vs. 85 %, respectively) [10]. However, this superiority was only true for cytology-based diagnoses: the with preserved tissue architecture adequate for histologic evaluation, and (iii) sample cellularity. Results: A total of 214 patients were enrolled. Compared to the first pass with a standard needle (n =108), the first pass with the (n =106) provided samples that were more often adequate for histologic evaluation (81.1 % vs %; P =0.048) and had superior cellularity (rich/moderate/poor, 36 %/27 %/37 % vs. 19 %/26 %/ 55 %; P =0.003). There were no significant differences between the two needles in sensitivity (75.6 % vs %, P=0.337) and accuracy (79.2 % vs %, P =0.561) for the diagnosis of malignancy. Conclusions: In patients with solid pancreatic masses, a 25-gauge EUS-FNA needle with a core trap provides histologic samples of better quality than a standard 25-gauge needle. There was no difference in accuracy for the diagnosis of malignancy between the needles. Clinical trial number: UMIN gauge needle was inferior to the 22-gauge needle in terms of the accuracy of histologybased diagnosis [11]. This probably reflects the fact that 25-gauge needles usually generate smaller sample volumes than 22-gauge and 19-gauge needles [12]. Rapid on-site evaluation (ROSE) is needed to confirm that the EUS-FNA samples are satisfactory for pathologic diagnosis and to decrease the number of passes, although it is controversial whether ROSE impacts on diagnostic accuracy [13, 14]. In order to decrease the number of passes, the adequacy of the sample obtained by each pass needs to be improved. To achieve this, a needle with a core trap was recently developed [15 20]. Compared with the standard needle, the needle with a core trap reduced the number of passes needed to establish a diagnosis, particularly a histology-based diagnosis; however, the diagnostic accuracy and diagnostic yield of the two needles were not significantly different [17, 19]. A retro-
2 633 spective study focused on the utility of the 25-gauge needle with a core trap and showed excellent cytology-based diagnostic yield for a single pass [20]. The aim of this prospective multicenter randomized controlled trial was to compare the novel 25-gauge needle with a core trap to a standard 25-gauge needle in terms of their ability to provide samples with preserved tissue architecture adequate for histologic evaluation and diagnosis in patients with pancreatic masses. Patients and methods Study design and patient enrollment This multicenter parallel-arm randomized study was approved by the Institutional Review Board of each participating hospital. All patients provided written informed consent. The trial was registered by the University hospital Medical Information Network: number UMIN All consecutive patients with solid pancreatic masses who presented to eight referral centers in Japan for EUS-FNA between April and September 2013 were prospectively enrolled through a designated website. Patients were included if they had a solid pancreatic mass as shown by imaging modalities, had no severe comorbidities, required a pathologic diagnosis to determine their treatment, and provided written informed consent. Patients were excluded from the study if they had a high risk of bleeding or did not provide informed consent. An EUS was performed to check for interposing vessels and problems with tumor visualization prior to randomization. Patients in whom such issues were found were also excluded from the study. The included patients were randomly assigned to two groups with a 1:1 ratio using a random number generator. One group underwent EUS-FNA with the novel 25-gauge needle with a core trap (EchoTip ProCore, Cook Medical, Bloomington, Indiana, USA), while the other group underwent EUS-FNA with a standard 25- gauge needle (EchoTip Ultra, Cook Medical). The two groups were designated as the ProCore and standard needle groups, respectively. Outcome measures For the purpose of this study, only samples obtained with the first needle pass were analyzed and used for comparisons of: (i) accuracy for the diagnosis of malignancy (primary outcome), (ii) rate of samples with preserved tissue architecture adequate for histologic evaluation, and (iii) sample cellularity (secondary outcomes). EUS-FNA technique EUS-FNA was performed using a linear array echoendoscope (GF- UCT 240 or GF-UCT 260, Olympus Optical, Tokyo, Japan; or EG- 530UT2, FUJIFILM, Tokyo, Japan) with the patient under conscious sedation. The same EUS-FNA technique was used in both groups. After the mass had been punctured, the stylet was slowly pulled out without suction (i. e. the slow-pull technique) while fanning the needle 20 times to and fro within the lesion. Samples were expelled into formalin bottles with the stylet and were processed for histologic analysis; ROSE was not performed. The sample was not split for cytologic, cell block, and histologic examination. To ensure that each patient would receive an accurate diagnosis, additional needle passes were then performed until the endosonographer felt that a sufficient sample had been obtained. Because these additional passes were not analyzed in this study, a technique different from that described above for the first pass could be used. Tissue processing and histologic assessment All formalin-fixed samples were brought to one designated facility 1 day after harvest and were processed for histologic evaluation. The same technique was used with each sample ( " Fig. 1). The entire formalin-fixed sample was spread onto a mesh sheet and stained by mercurochrome for easy recognition during processing. The samples were then dehydrated and embedded in paraffin. After the block had been cooled slightly, the mesh sheet was removed to yield the completed paraffin block. Ten slides bearing serial sections were prepared, two of which were stained with hematoxylin and eosin (H&E), the remaining eight slides being stained immunohistochemically. Two pathologists (S. Y. and A.Y.), blinded to the type of needle used, independently assessed all samples for: (i) cellularity, (ii) preservation of tissue architecture, and (iii) histologic diagnosis. Sample cellularity was classified as rich ( 5000 cells), moderate ( cells), or poor (<100 cells) ( " Fig.2). The pathologists conferred until a consensus was reached. The pathologists responsible for this study had experience of examining cytology and histology in more than 1000 EUS-FNA cases. Final diagnosis In patients who underwent surgical resection of the mass, the final diagnosis was based on surgical pathology. Patients who did not undergo surgical resection were followed up for at least 12 months with ultrasound, computed tomography (CT), magnetic resonance imaging (MRI), and/or EUS every 2 6 months or until their time of death. Patients were diagnosed with malignant disease if metastatic lesions were identified during imaging examinations, there were signs of disease progression, and/or malignant EUS-FNA results were obtained after the additional passes (the EUS-FNA results of the first pass were not used to determine the final diagnosis). Non-resected patients who did not display these imaging features during follow-up and had no EUS-FNA results suggesting malignancy after additional passes were diagnosed as having benign disease. Serous cyst neoplasm, neuroendocrine tumor (NET) G1, NET G2, and solid pseudopapillary neoplasm (SPN) were considered benign, whereas pancreatic carcinoma, NET G3, lymphoma, and metastases to the pancreas were considered malignant. Statistical analysis On the basis of previous reports [12,19], it was estimated that the diagnostic accuracy (the primary outcome) would be 80 % and 60 % in the ProCore and standard needle groups, respectively. Normal approximation revealed that given this difference, a type I error of 0.05, and power of 80 %, a sample of 100 patients per group would be required. Assuming a 5 % drop-out rate, a target sample size of 210 patients was established. The two groups were compared in terms of categorical and continuous variables using the chi-squared test (unless any expected value was less than 5, in which case Fisher s exact test was used) and t test (unless a Kolmogorov-Smirnov test indicated that the variable was not normally distributed, in which case a Wilcoxon s rank sum test was used), respectively. For the evaluation of sample cellularity, the Cochran-Armitage test was used. The Bre-
3 634 Fig. 1 The processing of samples for histologic evaluation. a Samples from endoscopic ultrasound-guided fine needle aspiration were inserted into formalin bottles; b the whole sample was spread onto a mesh sheet; c the sample was stained by mercurochrome for easy recognition during processing; d it was dehydrated and embedded in paraffin; e the mesh sheet was removed after the block had been allowed to cool slightly. f The completed paraffin block. slow Day test for the homogeneity of the odds ratios was performed prior to performing subgroup analysis. All statistical analyses were performed using SAS software version 9.1 (SAS Institute, Cary, North Carolina, USA). Results " Fig. 3 shows the study flow chart. Of the 225 consecutive patients with a pancreatic mass who presented for EUS-FNA during the study period, 214 patients were enrolled, while 11 were excluded for the following reasons: no informed consent (n = 7), high risk of bleeding (n=2), intervening vessels in the puncture route (n=1), and poor visualization of the tumor on EUS (n = 1). A total of 106 and 108 patients were randomized into the Pro- Core and standard needle groups, respectively. The groups did not differ significantly in terms of their demographic characteristics, mean tumor size, and puncture site ( " Table 1). " Table 2 shows the patients final diagnoses. These diagnoses were based on histologic examination of resected specimens in 61 patients, and on the clinical course/imaging analyses undertaken during follow-up in combination with EUS-FNA results of additional passes in 153 patients. The median follow-up period of those patients followed up was 358 days (range, days). The ProCore and standard needle groups did not differ significantly in the number of patients with final diagnoses of pancreatic adenocarcinoma (78 % and 72 %, respectively; P =0.303) and pancreatic malignancy (85 % and 78 %, respectively; P= 0.181). There were no significant complications during or after the EUS- FNA procedure in either group. The technical success rate (i. e. the successful puncture of the pancreatic mass on the first pass) in both groups was 100 %. " Table3 shows data on the quality of samples obtained in both groups. When compared with the standard needle, the first pass with the provided samples with preserved tissue architecture that were adequate for histologic evaluation significantly more frequently (81.1 % vs %; P = 0.048). Analysis of subgroups of patients punctured from the stomach and duodenum did not show significant differences between the groups. The cellularity of samples obtained with the was significantly superior to the cellularity of samples obtained with the standard needle (rich/moderate/poor cellularity, 36 %/27 %/ 37 % vs. 19 %/26 %/55 %; P = 0.003; " Table3). " Table 4 shows the performance characteristics of the first pass for the diagnosis of malignancy. No statistically significant differences in accuracy were found in either the analysis of all 214 patients or in the subgroup of 161 patients with samples adequate for histologic evaluation. The two pathologists differed in their view of whether there were adequate architectural features for diagnostic histology in five patients. Therefore, the agreement for this variable was 97.7 % and the kappa statistic was 93.9 %. The two pathologists also differed in terms of the diagnosis of malignancy in 10 patients, giving an agreement of 95.3% and kappa statistic of 90.5 % for this variable. Discussion The present study showed that in patients with a solid pancreatic mass, the first-pass samples obtained with the novel 25-gauge EUS-FNA needle with a core trap had a significantly better quality than the samples obtained with the standard 25-gauge needle, both in terms of sample cellularity and the rate of samples with preserved tissue architecture that permitted histologic evaluation. However, there was no significant difference between the two needles in terms of their diagnostic accuracy for the diagnosis of malignancy.
4 consecutive patients with pancreatic solid masses who presented to eight referral centers Excluded patients: n = 11 Intervening vessels (n = 1) Poor visualization of the tumor on EUS (n = 1) High risk of bleeding (n = 2) Refusal to participate in the study (n = 7) 214 patients enrolled in the study used n = 106 Standard EUS-FNA needle used n = 108 Fig. 3 Study flow chart. EUS-FNA, endoscopic ultrasound-guided fine needle aspiration. Fig. 2 Histologic views showing examples of different sample cellularities: a rich; b moderate; and c poor. Several studies have compared the performances of EUS-FNA needles with and without a core trap.hucl et al. [17] reported that in patients with pancreatic masses or lymphadenopathy, less needle passes were required to establish the diagnosis with the 22-gauge core needle than with the standard 22-gauge needle; however, the diagnostic accuracy of both needles was similar. Similarly, a randomized trial comparing a 22-gauge aspiration needle with a 22-gauge core-trap needle in 56 patients with solid pancreatic mass lesions revealed no significant differences in endpoints such as median number of passes required to establish the diagnosis, rates of diagnostic sufficiency, procurement of the histologic core, or the presence of diagnostic histologic specimens [18]. Increasing the number of passes from one to two and three did not significantly increase the sample adequacy and diagnostic accuracy. Lee et al. [19] also found that compared to a standard 22-gauge or 25-gauge needle, a 22-gauge or 25-gauge did not improve the overall diagnostic accuracy in pancreatic malignancy. However, the s did yield higher diagnostic accuracy and sensitivity when the samples were subjected to onsite cytology with the Diff-Quik stain. They also allowed more patients to be diagnosed with malignancy on the first pass. The advantages of our study include the fact that all of the samples were first-pass samples that were obtained by the same procedure, namely, the slow-pull technique. This technique was used in this study because it is associated with less contamination with blood and results in a higher diagnostic yield when a smaller (25- gauge or 22-gauge) core biopsy needle is used [20, 21]. This is also observed when slow-pull aspiration with a standard 25-gauge EUS-FNA needle is followed by either histologic diagnosis or cytology [22]. Other advantages of our study are that all of the samples were subjected to histologic analysis in a single facility staffed by experienced pathologists, all subjects were consecutive and randomized, and the pathologists were blinded to the type of needle used. Therefore, the study design prevented selection and information bias. In our study, we found that the first pass of the 25-gauge ProCore needle detected malignancy with a sensitivity of 75.6%. By contrast, Iwashita et al. [20] found that after a single pass with a 25- gauge core biopsy needle, histology detected malignancy in solid pancreatic lesions with a sensitivity of only 63 %, although it increased to 87 % after four passes (by contrast, cytologic analysis detected malignancy with a sensitivity of 83 % after one pass). It has been reported that seven passes are optimal for EUS-FNA of pancreatic lesions in terms of obtaining a correct diagnosis: the diagnostic sensitivity of this approach is 83 % [23]. However, the high quality of the tissue obtained by a single pass with the 25- gauge in the present study suggests that fewer passes may be needed when this needle is used. In our study, the technical success rates with the 25-gauge Pro- Core and standard needles were both 100 %, even though the transduodenal approach was used in 43 % (n = 93) of the patients. Moreover, the 25-gauge EUS-FNA yielded firstpass samples that retained architectural features in 81.1 % of the patients, and the overall diagnostic accuracy with the ProCore needle was 79.2 %. In contrast, Iglesias-Garcia et al. [15] found that EUS-FNA with a 19-gauge core biopsy needle did not yield adequate samples in 2 of their 35 patients with intraintestinal and extraintestinal masses who underwent EUS-FNA via the transduodenal approach. However, the 25-gauge core biopsy needle acquired adequate histologic samples less frequently than the 19-gauge core biopsy needle and its diagnostic accuracy was also lower. Similarly, Sakamoto et al. [11] found that EUS-guided 19-gauge Trucut needle biopsy followed by histologic analysis had an accuracy of 83.3 %,
5 636 Table1 Baseline characteristics of the 214 patients with pancreatic masses who underwent endoscopic ultrasound-guided fine needle aspiration. (n=108) Age, median (range), years 68 (43 90) 67 (34 89) Sex, male : female, n 53 : : Tumor size, mean ± SD, mm 29.3 ± ± Puncture site, stomach : duodenum, n 56 : : SD, standard deviation. Table2 Final diagnoses of the 214 patients with pancreatic masses who underwent endoscopic ultrasound-guided fine needle aspiration. (n=108) * Malignant disease, n (%) 90 (85 %) 84 (78 %) Adenocarcinoma Neuroendocrine tumor (grade 3) 2 0 Metastatic cancer 2 4 Acinar cell carcinoma 2 0 Malignant lymphoma 1 0 Intraductal papillary mucinous carcinoma 0 1 Cholangiocarcinoma 0 1 Benign disease, n (%) 16 (15 %) 24 (22 %) Chronic pancreatitis 4 8 Autoimmune pancreatitis 4 6 Neuroendocrine tumor (grade 1 or 2) 6 6 Solid pseudopapillary neoplasm 0 2 Serous cyst neoplasm 2 2 * for comparison of the frequencies of diagnoses in both groups of malignant/benign and adenocarcinoma/other disease. Table3 Quality of histologic samples obtained at the first needle pass. (n=108) Technical success rate 100 % (106/106) 100 % (108/108) Rate of samples adequate for histologic evaluation All patients, n = % (86/106) 69.4 % (75/108) Puncture from the stomach, n = % (43/56) 70.8 % (46/65) * Puncture from the duodenum, n= % (43/50) 67.4 % (29/43) * Sample cellularity Rich ( 5000 cells) 36 % (38/106) 19 % (21/108) Moderate ( cells) 27 % (29/106) 26 % (28/108) Poor (< 100 cells) 37 % (39/106) 55 % (59/108) * Subgroup comparisons were not performed because a Breslow Day test for homogeneity of the odds ratios was not significant (P=0.2445). Table4 Performance characteristics for the diagnosis of malignancy based on histologic evaluation of samples obtained at the first needle pass. All samples, n=214 Samples adequate for histologic evaluation, n=161 (n = 108) (n=86) (n=75) Sensitivity Specificity PPV NPV Accuracy 75.6 % (68/90) (72.4% 75.6%) 100 % (16/16) (82.5% 100%) 100 % (68/68) (82.5% 100%) 42.1 % (16/38) (34.7% 42.1%) 79.2 % (84/106) (74.0% 79.2%) 69.0% (58/84) (65.5 % 69.0 %) 100 % (24/24) (87.7 % 100%) 100 % (58/58) (94.9 % 100%) 48.0% (24/50) (42.1 % 48.0 %) 75.9% (82/108) (70.4 % 75.9 %) % (68/76) ( ) % (10/10) (75.8 % 100%) % (68/68) (96.4 % 100%) % (10/18) (42.1 % 55.6 %) % (78/86) (85.1 % 90.7 %) 93.5 % (58/62) ( ) 100% (13/13) (81.9% 100%) 100% (58/58) (95.9% 100%) 76.5 % (13/17) (62.6% 76.5%) 94.7 % (71/75) (88.4% 94.7%) CI, confidence interval; PPV, positive predictive value; NPV, negative predictive value.
6 637 whereas EUS-FNA with a 25-gauge needle followed by histology detected malignancy in solid pancreatic masses with poor accuracy (45.8 %). However, they did not examine which needle was better in terms of tissue acquisition and diagnostic yield. This study has several limitations. First, the final diagnoses of only 61 of the patients were determined by histology after surgical resection; the remaining 153 patients did not undergo surgery and therefore had to be diagnosed on the basis of their clinical course during the > 12-month follow-up period (diseasespecific death or signs of disease progression). Second, cytology, including ROSE, was not assessed; however, in the present study, we used the whole sample obtained by the first pass for the histologic examination because the aim of our study was to compare the diagnostic accuracy of EUS-FNA with the two needles by a simple standard method. Third, the results of the samples obtained by the additional passes after the first pass were not analyzed. The first pass (single pass) is not sufficient to diagnose pancreatic tumors. At present, best practice with respect to EUS-FNA requires multiple passes [14]. In this study, only the first-pass data were evaluated so as to examine whether the core trap impacted diagnostic accuracy under a simple set of conditions using strictly standardized methods. The imaging results and follow-up outcomes in combination with the later passes were used to determine the final diagnoses in patients who did not undergo surgery. Therefore, we did not use data from the later passes for a- nalysis. We found that the first pass with the yielded more tissue than the first pass with the standard needle, although there was no significant difference between the two in terms of sensitivity and accuracy. Therefore, the was superior to the standard needle only in terms of diagnostic yield. Several randomized controlled trials have compared Pro- Core needles with standard needles and all show that fewer passes are needed to establish the diagnosis when using the ProCore needle [17 19]; however, no reports have shown that the diagnostic accuracy and diagnostic yield are different. In conclusion, in patients with solid pancreatic masses, the quality of histologic samples obtained at the first pass with 25-gauge EUS-FNA needles with a core trap is better than the quality of samples obtained with standard 25-gauge needles. Samples obtained with the core needle have better cellularity and are more often adequate for histologic evaluation. However, better sample quality does not translate into improved accuracy for the diagnosis of malignancy, which is similar for both needle types. Competing interests: None Institutions 1 Department of Gastroenterology and Hepatology, Kinki University Faculty of Medicine, Osaka-sayama, Japan 2 Department of Surgical Pathology, Kyoto Prefectural University of Medicine, Kyoto, Japan 3 Clinical Research Center, Kinki University Hospital, Osaka-sayama, Japan 4 The Second Department of Internal Medicine, Osaka Medical College, Takatsuki, Japan 5 Department of Cancer Survey and Gastrointestinal Oncology, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka, Japan 6 Department of Gastroenterology, Osaka City General Hospital, Osaka, Japan 7 Department of Gastroenterology, Bell Land General Hospital, Sakai, Japan 8 Digestive Disease Center, Kitano Hospital, Osaka, Japan 9 The Third Department of Internal Medicine, Kansai Medical University, Hirakata, Japan 10 Department of Gastroenterology and Hepatology, Osaka Red Cross Hospital, Osaka, Japan Acknowledgments This study was supported by grants from the Japan Society for Promotion of Science (no and ). 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