Endoscopy 2023; 55(03): 225-234
DOI: 10.1055/a-1915-1812
Original article

Wet-suction versus slow-pull technique for endoscopic ultrasound-guided fine-needle biopsy: a multicenter, randomized, crossover trial

 1   Digestive Endoscopy Unit, The Pancreas Institute, G.B. Rossi University Hospital, Verona, Italy
,
Maria Cristina Conti Bellocchi
 1   Digestive Endoscopy Unit, The Pancreas Institute, G.B. Rossi University Hospital, Verona, Italy
,
Roberto Di Mitri
 2   Gastroenterology and Endoscopy Unit, Arnas Civico Di Cristina Benfratelli Hospital, Palermo, Italy
,
Frediano Inzani
 3   Pathology Unit, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
,
Mihai Rimbaș
 4   Gastroenterology Department, Clinic of Internal Medicine, Colentina Clinical Hospital, Carol Davila University of Medicine, Bucharest, Romania
,
 5   Gastroenterology Unit, Hospital of Imola, University of Bologna, Imola, Italy
,
Guido Manfredi
 6   Gastroenterology and Digestive Endoscopy Department, ASST Ospedale Maggiore Crema, Crema, Italy
,
 7   Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong
,
 8   Gastrointestinal Endoscopy Unit, Humanitas Mater Domini, Castellanza, Italy
 9   Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy
,
Oriol Sendino
10   Endoscopy Unit, Department of Gastroenterology, Hospital Clínic Barcelona, IDIBAPS, CIBEREHD, University of Barcelona, Barcelona, Spain
,
Laura Bernardoni
 1   Digestive Endoscopy Unit, The Pancreas Institute, G.B. Rossi University Hospital, Verona, Italy
,
Erminia Manfrin
11   Department of Diagnostics and Public Health, G.B. Rossi University Hospital, Verona, Italy
,
 2   Gastroenterology and Endoscopy Unit, Arnas Civico Di Cristina Benfratelli Hospital, Palermo, Italy
,
Elettra Unti
12   Pathology Unit, ARNAS Civico Di Cristina Benfratelli Hospital, Palermo, Italy
,
Angela Carlino
 3   Pathology Unit, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
,
Theodor Voiosu
 4   Gastroenterology Department, Clinic of Internal Medicine, Colentina Clinical Hospital, Carol Davila University of Medicine, Bucharest, Romania
,
R. Bogdan Mateescu
 4   Gastroenterology Department, Clinic of Internal Medicine, Colentina Clinical Hospital, Carol Davila University of Medicine, Bucharest, Romania
,
 5   Gastroenterology Unit, Hospital of Imola, University of Bologna, Imola, Italy
,
Stefania Lega
13   Pathology Unit, Hospital of Imola, Imola, Italy
,
Elisabetta Buscarini
 6   Gastroenterology and Digestive Endoscopy Department, ASST Ospedale Maggiore Crema, Crema, Italy
,
Lorena Pergola
14   Pathology Department, ASST Ospedale Maggiore Crema, Crema, Italy
,
 7   Department of Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong
,
 8   Gastrointestinal Endoscopy Unit, Humanitas Mater Domini, Castellanza, Italy
,
Àngels Ginès
10   Endoscopy Unit, Department of Gastroenterology, Hospital Clínic Barcelona, IDIBAPS, CIBEREHD, University of Barcelona, Barcelona, Spain
,
Gloria Fernández-Esparrach
10   Endoscopy Unit, Department of Gastroenterology, Hospital Clínic Barcelona, IDIBAPS, CIBEREHD, University of Barcelona, Barcelona, Spain
,
 1   Digestive Endoscopy Unit, The Pancreas Institute, G.B. Rossi University Hospital, Verona, Italy
15   Department of Medical and Surgical Sciences, Section of Gastroenterology, University of Foggia, Foggia, Italy
,
Alberto Larghi
16   Digestive Endoscopy Unit, Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy
› Author Affiliations
Trial Registration: ClinicalTrials.gov Registration number (trial ID): NCT04834193 Type of study: Prospective, randomized, multi-center, cross-over study
 


Abstract

Background It is unknown whether there is an advantage to using the wet-suction or slow-pull technique during endoscopic ultrasound-guided fine-needle biopsy (EUS-FNB) with new-generation needles. We aimed to compare the performance of each technique in EUS-FNB.

Methods This was a multicenter, randomized, single-blind, crossover trial including patients with solid lesions of ≥ 1 cm. Four needle passes with 22 G fork-tip or Franseen-type needles were performed, alternating the wet-suction and slow-pull techniques in a randomized order. The primary outcome was the histological yield (samples containing an intact piece of tissue of at least 550 μm). Secondary end points were sample quality (tissue integrity and blood contamination), diagnostic accuracy, and adequate tumor fraction.

Results Overall, 210 patients with 146 pancreatic and 64 nonpancreatic lesions were analyzed. A tissue core was retrieved in 150 (71.4 %) and 129 (61.4 %) cases using the wet-suction and the slow-pull techniques, respectively (P = 0.03). The mean tissue integrity score was higher using wet suction (P = 0.02), as was the blood contamination of samples (P < 0.001). In the two subgroups of pancreatic and nonpancreatic lesions, tissue core rate and tissue integrity score were not statistically different using the two techniques, but blood contamination was higher with wet suction. Diagnostic accuracy and tumor fraction did not differ between the two techniques.

Conclusion Overall, the wet-suction technique in EUS-FNB resulted in a higher tissue core procurement rate compared with the slow-pull method. Diagnostic accuracy and the rate of samples with adequate tumor fraction were similar between the two techniques.


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Introduction

Endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) has become an essential tool for the diagnosis of solid pancreatic and nonpancreatic lesions, with 85 % sensitivity and 98 % specificity [1]. Several factors have been previously evaluated to optimize outcomes of EUS-FNA [1], such as use of rapid on-site evaluation (ROSE) for immediate cytopathological assessment [2] [3], use of needles of different calibers and types [4], number of needle passes [5], and different sampling techniques [6].

In the past decade, new EUS needles for the acquisition of histological specimens (fine-needle biopsy [EUS-FNB]) have been developed to overcome the limitations of cytology, facilitating the differential diagnosis of rare conditions through performance of specific immunohistochemical staining [7], and obviating the need for ROSE [8]. Two end-cutting needles (i. e. fork-tip SharkCore needle, Covidien/Medtronic, Boston, Massachusetts, USA; and the Franseen-type needle, Acquire, Boston Scientific, Marlborough, Massachusetts, USA) have shown excellent histological yields [9] [10], with comparable diagnostic performance in two randomized controlled trials (RCTs) and two metanalyses [11] [12] [13] [14]. Importantly, EUS-FNB samples have been demonstrated to be suitable for next-generation sequencing [15] when containing a tumor fraction of ≥ 20 %, either for pancreatic ductal adenocarcinoma (PDAC) [16] or pancreatic neuroendocrine tumors (pNETs) [17]. Consequently, current practice has almost completely shifted from EUS-FNA to EUS-FNB [18].

Different sampling techniques have been introduced and compared with the standard suction technique, including the slow-pull and wet-suction techniques. With standard suction, the stylet is removed and an air-filled pre-vacuum 10 mL or 20 mL syringe is attached to the proximal end of the needle and opened once inside in the lesion to apply negative pressure suction [19]. In the slow-pull technique, negative pressure is created by slowly withdrawing the stylet from the needle [20]. In the wet-suction technique, the needle is flushed with saline to replace the column of air, and a pre-vacuum 10 mL or 20 mL syringe is utilized to apply suction [21]. The standard suction and slow-pull techniques have been widely studied for EUS-FNA. A recent meta-analysis, including seven RCTs comparing them for sampling of solid pancreatic lesions, demonstrated similar adequacy and accuracy, with less blood contamination for the slow-pull method [22]. The wet-suction technique has been introduced more recently and two RCTs comparing standard and wet suction for EUS-FNA reported significant higher specimen cellularity, adequacy, and accuracy with wet suction, both for solid pancreatic and nonpancreatic lesions [21] [23].

To date, a single-center pilot RCT has evaluated different sampling techniques on EUS-FNB of solid pancreatic lesions, comparing standard, slow-pull, and wet-suction methods, using both the fork-tip and Franseen-type needles. No difference in cellularity scores or blood contamination were found, regardless of the technique or needle type used [24]. However, the small sample size, inclusion of only solid pancreatic lesions, and the single-center design did not allow definitive conclusions to be drawn, leaving these issues still open for further evaluation.

We performed a multicenter RCT with the primary aim of comparing the histological yield of EUS-FNB using the slow-pull and wet-suction techniques in patients with pancreatic and nonpancreatic solid lesions. Secondary aims included evaluation of sample quality, tumor fraction, and diagnostic accuracy.


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Methods

Study design

This study was an international, single-blinded, crossover, randomized study involving nine centers. It was first approved by the ethics committee of the provinces of Verona and Rovigo on 29 March 2021 (protocol number 18440), and subsequently by ethics committees and institutional review boards of all participating centers. All patients signed informed consent before inclusion into the study.


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Patient population

Consecutive adult patients with a solid lesion of ≥ 1 cm who were referred for EUS evaluation and were able to provide informed consent were assessed for study eligibility. Patients with bleeding disorders (uncorrectable with coagulation factors or fresh frozen plasma), concomitant anticoagulants use (not to be discontinued), an international normalized ratio of > 1.5, platelet count of < 50 000, pregnant or breastfeeding, lesions with cystic component (> 50 % of the volume), or included in another study, were excluded.


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EUS procedure and specimen processing

EUS procedures were performed by expert endosonographers without involvement of trainees. Once the target lesion was visualized on EUS, interposed vessels were excluded using color Doppler. A 22 G end-cutting needle, fork-tip or Franseen-type, was used in all cases, with the choice of needle type left to the endosonographer’s discretion or according to availability at each center. Four passes were performed using the same needle, alternating the sampling techniques according to the randomization list (see below). During each pass, regardless of the sampling procedure, approximately 10 to-and-fro movements of the needle were performed inside the lesion, utilizing the fanning technique whenever possible [25]. For wet suction, the stylet was removed and the needle pre-flushed with 1–2 mL of saline. The lesion was then punctured, and suction applied using a 10 mL pre-vacuum syringe [23]. For the slow-pull method, after puncturing the lesion, the stylet was slowly and gradually withdrawn for at least 40 cm. The samples collected were finally pushed into two formalin vials. The samples retrieved with the same sampling technique (i. e. 1st/3 rd passes and 2nd/4th passes) were placed in the same container. Specimens were processed as standard biopsies (e. g. after being embedded in paraffin, sections of 5 μm thickness were cut from paraffin blocks and stained with hematoxylin and eosin). ROSE was not used in any case. Patients were excluded if the lesion was impossible to puncture and dropped out if at least one needle pass with each technique was not performed.


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Randomization and blinding

Once the eligibility for inclusion into the trial was verified, patients were randomized in a 1:1 ratio in a crossover design into Group A and Group B, based on a computer-generated randomized block sequence (block size of 10). For Group A, the pass sequence was wet suction, slow pull, wet suction, slow pull. For Group B, the pass sequence was slow pull, wet suction, slow pull, wet suction. The randomization list was stratified by the type of lesion (pancreatic vs. nonpancreatic).

A data manager not involved in the data analysis or patient enrollment generated the randomization list. At each center, sealed envelopes containing the group assignment were prepared and opened after obtaining study consent and EUS baseline assessment, just prior to EUS-FNB.

The pathologists designated for sample evaluation were blinded to patients’ randomization and type of EUS-FNB technique performed during the entire study.


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Definition of study end points

Primary end point

The primary end point was the tissue core procurement rate. A tissue “core” was defined as at least one intact piece of tissue of 550 μm or more in length [26] [27]. The length of histological fragments was measured using dedicated software at each participating center.


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Secondary end points

Sample quality was evaluated in terms of tissue integrity and blood contamination, applying a previously utilized, simplified, score [28] [29] [30] [31]. Briefly, a score ranging from 0 to 3 was assigned to the specimens by a blinded pathologist. For both tissue integrity and blood contamination, the higher the score the better the sample quality ([Table 1]).

Table 1

Sample quality scores (tissue integrity and blood contamination).

Score

Tissue integrity

0

No cells/tissue

1

Cytological specimen (disaggregated cells representative of the target lesion not allowing for tissue architectural assessment)

2

Histological microfragments (sample adequate for histological evaluation, namely an architecturally intact piece of tissue but without a “core”)

3

Histological “core” (defined as an architecturally intact piece of tissue measuring at least 550 μm)

Score

Blood contamination

0

Only blood

1

High blood contamination (> 50 % of the surface of the slide)

2

Moderate blood contamination (25 %–50 % of the surface of the slide)

3

Low blood contamination (< 25 % of the surface of the slide)

The rate of samples containing an adequate tumor fraction was assessed for PDAC and pNET cases. Tumor fraction was considered adequate if the ratio of tumor cells in a background of benign nucleated cells exceeded 20 % [16] [17].

Diagnostic accuracy was measured as conventional “malignancy” analysis using strict criteria (i. e. samples reported as suspicious for malignancy were categorized as negative). Definitive diagnosis was assessed on surgical specimens whenever available, while in nonresected patients it was based on the diagnostic work-up (combined outcomes of imaging studies and any additional biopsy sample result) and clinical course of the disease of at least 6 months [32]. Follow-up was performed by the study investigators at each center by outpatient visits, electronic chart review, and telephone contacts, and was terminated in case of surgical resection or death. The Papanicolaou classification [33] was used to classify both EUS-FNB samples and surgical specimens of pancreatic masses. Low grade tumors (e. g. neuroendocrine tumor, solid pseudopapillary tumor) were considered malignant. Lymph nodes were simply classified as benign or malignant. Specimens that contained inadequate material were considered as negative for malignancy.


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Sample size

The sample size was calculated in the context of the primary binary outcome and considering the crossover study design with each lesion sampled using the two techniques. Assuming an expected pooled histological yield of 95 % with wet suction [23] and 85 % with slow pull [34] [35], with α = 0.05, power = 0.9, and calculating the proportion of discordant pairs (equal to 0.18) with the approximation of Machin D et al. [36] due to the lack of data in the current literature, the total required sample size was established to be of 185 patients. Assuming an approximate 8 % drop-out rate, a sample size of 200 patients was initially calculated. After the study was initiated, some concerns about a potential higher drop-out rate were raised. Therefore, an amendment to the protocol was made and the drop-out rate was increased to 20 %, resulting in a final sample size of 220 patients.


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Statistical analysis

The characteristics of the samples were summarized by descriptive statistics (mean with SD for continuous variables and frequency distributions for categorical variables). The follow-up time in nonresected patients was reported as median with 95 %CI.

Rate of tissue cores, samples containing an adequate tumor fraction, and diagnostic accuracy (defined as true positive + true negative divided by total number of patients) were compared using McNemar test, whereas tissue quality scores were compared by means of Wilcoxon signed-rank test. All the analyses were performed in the overall cohort and in the subgroups of pancreatic and nonpancreatic lesions. A Bonferroni correction for multiple comparisons was applied in the subgroup analyses. A further sub-analysis concerning the primary outcome was performed according to the different needles utilized. Both intention-to-treat (i. e. including all patients who underwent at least one needle pass with each technique) and per-protocol (i. e. two passes with each technique were performed) analyses were scheduled.

In order to account for eventual center effects in the analysis, a random-effects analysis fitting a logistic regression model was performed according to the formula

log it (πij) = α + βtreatXij + uj,

where πij is the probability of an event for the ith patient in the jth center, βtreat indicates the log odds ratio for treatment, Xij indicates whether the patient received the treatment or control, and uj is the effect of the jth center [37].

All analyses were performed using R Statistical Software 3.0.2 (Foundation for Statistical Computing, Vienna, Austria) with a statistical level of significance of 5 % and respective 95 %CIs. Sample size calculation was performed with R Statistical Software 3.0.2 (pwr package). A two-tailed distribution was used and statistical significance was considered for P  < 0.05.


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Results

Between April 2021 and October 2021, 244 patients were assessed for eligibility. A total of 24 patients were excluded and 220 underwent EUS-FNB. Two and eight patients in groups A and B, respectively, dropped out due to the inability to perform the second needle pass as a result of the onset of anesthesiological complications in three patients (desaturation in two cases and bradycardia in one) and perilesional self-limiting hematoma in seven cases. Consequently, a strict intention-to-treat analysis was not possible due to the lack of comparative samples in these cases, and therefore only a per-protocol analysis was performed. No protocol deviation occurred in the analyzed patients.

A total of 210 patients (mean age 65.9 [SD 11.3] years; 55.5 % male) were analyzed: 108 in Group A and 102 in Group B. The flow chart of the study is presented in [Fig. 1]. No differences in patient demographics and lesion characteristics were observed ([Table 2]). Overall, there were 146 pancreatic and 64 nonpancreatic lesions, with a mean size of 35.1 (SD 17.5) mm.

Zoom Image
Fig. 1 CONSORT flow chart of the study [38]. EUS, endoscopic ultrasound.
Table 2

Patient demographic details, lesion characteristics, procedures performed, and outcomes in 210 patients who underwent endoscopic ultrasound-guided fine-needle biopsy performed using the wet-suction and the slow-pull sampling techniques.

Variable

Overall (n = 210)

Group A (wet suction first) (n = 108)

Group B (slow pull first) (n = 102)

P value

Age, mean (SD), years

65.9 (11.3)

65.4 (12.0)

66.4 (10.5)

0.51

Sex, n (%)

0.70

  • Male

114 (54.3)

60 (55.6)

54 (52.9)

  • Female

96 (45.7)

48 (44.4)

48 (47.1)

Lesion site, n (%)

0.17

Submucosal

18 (8.6)

7 (6.5)

11 (10.8)

  • Esophagus

1

0

1

  • Stomach

13

6

7

  • Duodenum

3

0

3

  • Rectum

1

1

0

Pancreatic

146 (69.5)

72 (66.7)

74 (72.5)

  • Head/uncinate

80

35

45

  • Neck/body

46

27

19

  • Tail

20

10

10

Lymph node

20 (9.5)

13 (12.0)

7 (6.9)

Other

26 (12.4)

16 (14.8)

10 (9.8)

  • Retroperitoneum

8

5

3

  • Liver

8

4

4

  • Adrenal

4

4

0

  • Rectum (perianastomotic granuloma)

1

1

0

  • Lung

2

1

1

  • Pelvic

1

0

1

  • Gallbladder

1

0

1

  • Spleen

1

1

0

Lesion size, mean (SD), mm

35.1 (17.5)

33.5 (17.6)

36.7 (17.3)

0.18

Needle type, n (%)

0.25

  • Fork-tip 22 G

124 (59.0)

63 (58.3)

61 (59.8)

  • Franseen-type 22 G

86 (41.0)

45 (41.7)

41 (40.2)

Use of fanning technique, n (%)

183 (87.1)

93 (86.1)

90 (88.2)

0.31

Follow-up

0.20

  • Surgical resection, n (%)

42 (20.0)

18 (16.7)

24 (23.5)

  • Evaluation of clinical course, n (%)

168 (80.0)

90 (83.3)

78 (76.5)

  • Follow-up in non-resected patients, median (95 %CI), days

187 (141–225)

191 (142–228)

183 (140–222)

Final diagnosis, n (%)

0.77

  • Pancreatic ductal adenocarcinoma

113 (53.8)

53 (49.1)

60 (58.8)

  • Pancreatic neuroendocrine tumor

19 (9.0)

10 (9.3)

9 (8.8)

  • Pancreatitis

9 (4.3)

6 (5.6)

3 (2.9)

  • GIST

13 (6.2)

6 (5.6)

7 (6.9)

  • Liver metastasis

6 (2.9)

3 (2.8)

3 (2.9)

  • Retroperitoneal cancer

6 (2.9)

3 (2.8)

3 (2.9)

  • Malignant lymph node

18 (8.6)

12 (11.1)

6 (5.9)

  • Other[*]

26 (12.4)

15 (13.9)

11 (10.8)

IQR, interquartile range; GIST, gastrointestinal stromal tumor.

* Other includes: pancreatic metastasis (3), intrahepatic cholangiocarcinoma (2), leiomyoma (2), lipoma (2), benign lymph node (2), lung cancer (2), benign adrenal nodule (2), adrenal metastasis (2), gallbladder cancer (1), spleen lymphoma (1), cervical cancer (1), retroperitoneal schwannoma (1), retroperitoneal lymphoepithelial cyst (1), pancreatic solid pseudopapillary neoplasm (1), pancreatic serous cystadenoma (1), duodenal neuroendocrine tumor (1), perianastomotic rectal granuloma (1).


Primary outcome

Results of the primary outcome are shown in [Table 3]. Overall, a tissue core was obtained in 71.4 % and 61.4 % of patients using the wet-suction and slow-pull techniques, respectively (P = 0.03). According to the random-effects model adjusted for center effects, the odds ratio (OR) for tissue core acquisition was 1.58 (95 %CI 1.05–2.38; P = 0.03). No difference for the primary outcome in the subgroup analysis of solid pancreatic lesions (73.3 % vs. 67.1 %, respectively; P = 0.25) and in the subgroup of nonpancreatic lesions (67.2 % vs. 48.4 %, respectively; P = 0.03 with a significance threshold set at 0.025 based on Bonferroni adjustment for multiple comparisons) was observed between the wet-suction and slow-pull techniques, respectively.

Table 3

Results of the primary and secondary aims in the overall cohort and in the subgroups of patients with solid pancreatic and nonpancreatic lesions who underwent endoscopic ultrasound-guided fine-needle biopsy performed using the wet-suction and slow-pull sampling techniques.

Wet suction

Slow pull

P value

Presence of tissue core[1], n (%)

  • Overall population (n = 210)

150 (71.4)

129 (61.4)

0.03

  • Pancreatic lesions (n = 146)

107 (73.3)

98 (67.1)

0.25[2]

  • Nonpancreatic lesions (n = 64)

43 (67.2)

31 (48.4)

0.03[2]

Tissue integrity score, mean (SD)

  • Overall population (n = 210)

2.63 (0.62)

2.48 (0.74)

0.02

  • Pancreatic lesions (n = 146)

2.66 (0.61)

2.55 (0.71)

0.16[2]

  • Nonpancreatic lesions (n = 64)

2.57 (0.66)

2.30 (0.79)

0.04[2]

Blood contamination score, mean (SD)

  • Overall population (n = 210)

2.09 (0.81)

2.44 (0.74)

< 0.001

  • Pancreatic lesions (n = 146)

2.15 (0.77)

2.45 (0.74)

< 0.001[2]

  • Nonpancreatic lesions (n = 64)

1.95 (0.88)

2.42 (0.75)

< 0.001[2]

Adequate tumor fraction rate[3], n/N (%)

112/132 (84.8)

106/132 (80.3)

0.41

Diagnostic accuracy, n (%)

  • Overall population (n = 210)

192 (91.4)

183 (87.1)

0.16

  • Pancreatic lesions (n = 146)

132 (90.4)

126 (86.3)

0.28[2]

  • Nonpancreatic lesions (n = 64)

60 (93.7)

57 (89.1)

0.64[2]

1 Intact piece of tissue of at least 550 µm.


2 Based on Bonferroni correction for multiple comparisons, significance threshold was set at 0.025 in subgroup analysis.


3 Tumor fraction rate was evaluated including only cases of pancreatic ductal adenocarcinomas and neuroendocrine tumors.


The study population was further stratified according to the needle type. The two needles showed similar performance in obtaining a tissue core based on sampling technique for both solid pancreatic lesions (fork-tip needle: 54/82 (65.9 %) for wet suction vs. 54/82 (65.9 %) for slow pull, P > 0.99; Franseen-type needle: 53/64 (82.8 %) for wet suction vs. 44/64 (68.8 %) for slow pull, P = 0.09) and nonpancreatic lesions (fork-tip needle: 26/42 (61.9 %) for wet suction vs. 18/42 (42.9 %) for slow pull, P = 0.12; Franseen-type needle: 17/22 (77.3 %) for wet suction vs. 13/22 (59.1 %) for slow pull, P = 0.33).


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Secondary outcomes

Results of secondary outcomes are summarized in [Table 3]. Overall, tissue integrity score was higher with the wet-suction compared with the slow-pull technique (P = 0.02). Center effects-adjusted OR for tissue integrity score was 1.66 (95 %CI 1.12–2.41; P = 0.02). However, in the two subgroup analyses, the tissue integrity score was not significantly different between the two techniques (P = 0.16 and P = 0.04 for solid pancreatic lesions and nonpancreatic lesions, respectively, with a significance threshold set at 0.025 based on Bonferroni adjustment for multiple comparisons). The blood contamination score was higher among slow-pull specimens, both in the overall population, and in the pancreatic and nonpancreatic subgroups, respectively (P < 0.001). Center effects-adjusted OR for blood contamination score was 0.56 (95 %CI 0.12–0.81; P < 0.001).

The rate of samples with adequate tumor fraction was evaluated among the 132 cases of PDAC and pNETs, and was similar with wet-suction and slow-pull techniques (84.8 % vs. 80.3 %, respectively; P = 0.41). Based on random-effects model adjusted for center effects, the OR for adequacy of tumor fraction was 1.35 (95 %CI 0.70–2.55; P = 0.39).

Six and eight specimens were deemed not diagnostically adequate using the wet-suction and slow-pull techniques, respectively. Overall, among specimens collected using the wet-suction technique, there were 173 true positives, 19 true negatives, 0 false positives, and 18 false negatives, corresponding to a diagnostic accuracy of 91.4 % (95 %CI 86.8–94.8). Specimens collected using the slow-pull technique were assessed as 163 true positives, 20 true negatives, 0 false positives, and 27 false negatives, corresponding to a diagnostic accuracy of 87.1 % (95 %CI 81.5–91.4), with no significant difference between the two techniques (P = 0.16). Based on random-effects model adjusted for center effects, the OR for diagnostic accuracy was 1.58 (95 %CI 0.81–2.93; P = 0.16). Similarly, diagnostic accuracy was also comparable when evaluating the subgroup of solid pancreatic lesions (P = 0.28) and nonpancreatic lesions (P = 0.64).


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Discussion

Possible differences in tissue core procurement between available sampling techniques using fork-tip and Franseen-type needles have not been fully investigated. In 2021, Bang et al. published an RCT comparing standard suction vs. slow-pull technique vs. no suction with various types of needles [39]. This study showed that, in contrast to side-fenestrated reverse-bevel, and Menghini-tip needles, for Franseen-type and fork-tip needles there was no difference between the standard suction and slow-pull techniques, and neither technique significantly improved the rate of diagnostic adequacy and accuracy when compared with no suction [39]. However, the wet-suction method was not evaluated, and the potential advantage of this technique remains unknown. To better clarify this issue, we performed a randomized, crossover trial with the primary aim of comparing wet-suction and slow-pull techniques in their capability to acquire proper tissue “core” samples for histological evaluation.

In the overall study population evaluated in the present study, wet suction showed a higher rate of tissue core acquisition. However, this statistical difference was mainly related to the higher rate of tissue core retrieved in the subgroup of nonpancreatic lesions (67.2 % vs. 48.4 %). In this subgroup of patients, we also found that wet suction provided a higher tissue integrity score. For both outcomes, in this subgroup of patients, statistical significance was not reached but a trend toward significance was observed (P = 0.03 and P = 0.04 for tissue core rate and tissue integrity score, respectively, with a significance threshold set at 0.025 based on Bonferroni adjustment for multiple comparisons) and it is likely that, with a larger population, significance would have been achieved. In contrast, for solid pancreatic lesions, tissue core procurement rate and tissue integrity score were similar between the two techniques. The present study seems to support the findings of a previous pilot study comparing wet suction with slow pull and standard suction for sampling of solid pancreatic lesions using end-cutting needles, where all three techniques resulted in similar histological yields [24].

As previously described for EUS-FNA [22], slow-pull specimens resulted in lower blood contamination compared with wet-suction samples. This finding differs from the pilot study mentioned above, in which blood contamination was similar regardless of the sampling technique used [24]. However, the blood contamination score used was extremely simplified (score 0 = blood present and 1 = blood clots present), thus limiting the possibility of accurately differentiating and stratifying the results. On the other hand, the significance of blood contamination in the assessment of histological samples could be questioned. Indeed, no data demonstrated that blood contamination impairs diagnostic accuracy or the capability to retrieve histological tissue. Indeed, in the present study, samples collected using wet suction were highly contaminated with blood. Nevertheless, the other outcomes were similar to or even better than those obtained with the slow-pull technique.

In particular, diagnostic accuracy was slightly higher with wet suction for both solid pancreatic (90.4 % vs. 86.3 %) and nonpancreatic (93.7 % vs. 89.1 %) lesions, despite a significant difference not being observed. A similar result was observed for tumor fraction adequacy. Based on these results, in patients with solid pancreatic lesions, the choice of technique between slow pull and wet suction strongly depends on agreement with and preference of the pathologist, considering the lower blood contamination using the slow-pull method. In patients with nonpancreatic lesions, our study seems to favor the use of wet suction over slow pull due to the higher rates of tissue core acquisition, with higher tissue integrity score. However, our findings should be interpreted with caution for different reasons. First, the number of patients included may be insufficient to detect a significant difference in clinically important outcomes such as diagnostic accuracy. Second, we included all nonpancreatic lesions, and further confirmation in specifically designed and adequately powered studies focused on these types of lesions are needed. Nonetheless, to the best of our knowledge, this is the first study to compare wet-suction and slow-pull techniques for EUS-FNB of nonpancreatic lesions.

The difference we observed between solid pancreatic lesions and nonpancreatic lesions can be easily explained by the nature of the lesion biopsied. In fact, most solid pancreatic lesions were PDAC, which are characterized by a large amount of fibrous stroma increasing mass stiffness. Therefore, it is plausible that the end-cutting design of the needles used in this study allowed the coring of hard lesions such as PDACs regardless of the sampling technique. In contrast, nonpancreatic lesions are usually softer, and, therefore, the application of suction might have impacted the quantity of aspirated tissue into the needle. No differences in the primary outcome between the two needles used in this study were detected. This result is consistent with previous literature reporting the same performance of the fork-tip and Franseen-type needles [11] [12] [13] [14].

Our study has some limitations. First, all involved centers were highly experienced, and results might not be reproducible in other settings. Second, we excluded very small lesions because performing four needle passes on lesions of < 1 cm is often difficult and in the case of solid pancreatic lesions may increase the risk of acute pancreatitis. Therefore, we cannot be sure that our results would be similar in small lesions, especially considering the reported impact of lesion size on the outcome of EUS sampling [40]. Third, we used a single needle caliber, and our findings could be different with both larger and smaller needles. Fourth, both fork-tip and Franseen-type needles were used without randomization. Further studies, adequately powered, should investigate and compare the performance of these two needle types using different sampling techniques. Fifth, we included both pancreatic and nonpancreatic lesions, and subgroup analyses were performed. Because the performance of EUS-FNB can be different in pancreatic and nonpancreatic lesions, and this trial was not powered to compare the two techniques based on the lesion type, further studies are needed to properly evaluate this matter. Sixth, despite the quite large number of patients included, our study may not have been adequately powered, as the definitions of histological yield and tissue core are not standardized, and the sample size calculation was based on previous literature that reported a very high histological yield, which was different from the tissue core rate we observed in the present study. Finally, we did not evaluate the standard suction technique. However, a recent meta-analysis of EUS-FNA RCTs comparing the slow-pull technique with standard suction demonstrated similar adequacy, but lower blood contamination and slightly higher accuracy using the slow-pull technique, making this technique preferred over standard suction in modern practice [22].

In conclusion, our study demonstrated that EUS-FNB performed with wet suction provided a higher tissue core procurement rate than a slow-pull technique. Diagnostic accuracy and rate of samples with adequate tumor fraction were slightly higher using wet suction, but no statistically significant difference between the two techniques was observed. Further large, specifically powered, multicenter studies are needed to definitively recommend one of these two techniques.


#
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Competing Interest

S.F. Crinò has received speaker fees from Steris Endoscopy. A. Larghi is a consultant for Pentax and Boston Scientific, and has received a research grant from Medtronic and teaching fee from Taewoong. À. Ginès is a consultant for Cook Endoscopy. R. Di Mitri is a consultant for Boston Scientific. O. Sendino is a consultant for and has received speaker fees from B. Braun. M.C. Conti Bellocchi, F. Inzani, M. Rimbas, A. Lisotti, G. Manfredi, A.Y.B. Teoh, B. Mangiavillano, L. Bernardoni, E. Manfrin, D. Scimeca, E. Unti, A. Carlino, T. Voiosu, R.B. Mateescu, P. Fusaroli, S. Lega, E. Buscarini, L. Pergola, S.M. Chan, L. Lamonaca, G. Fernández-Esparrach, and A. Facciorusso declare that they have no conflict of interest.

  • References

  • 1 Dumonceau JM, Polkowski M, Larghi A. et al. European Society of Gastrointestinal Endoscopy. Indications, results, and clinical impact of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline. . Endoscopy 2011; 43: 897-912
  • 2 Hikichi T, Irisawa A, Bhutani MS. et al. Endoscopic ultrasound-guided fine-needle aspiration of solid pancreatic masses with rapid on-site cytological evaluation by endosonographers without attendance of cytopathologists. J Gastroenterol 2009; 44: 322-328
  • 3 Polkowski M, Jenssen C, Kaye P. et al. Technical aspects of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Technical Guideline – March 2017. Endoscopy 2017; 49: 989-1006
  • 4 Bang JY, Navaneethan U, Hasan MK. et al. Endoscopic ultrasound-guided specimen collection and evaluation techniques affect diagnostic accuracy. Clin Gastroenterol Hepatol 2018; 16: 1820-1828
  • 5 Erickson RA, Sayage-Rabie L, Beissner RS. Factors predicting the number of EUS-guided fine-needle passes for diagnosis of pancreatic malignancies. Gastrointest Endosc 2000; 51: 184-190
  • 6 Wani S. Basic techniques in endoscopic ultrasound-guided fine needle aspiration: role of a stylet and suction. Endosc Ultrasound 2014; 3: 17-21
  • 7 Crinò SF, Bernardoni L, Manfrin E. et al. Endoscopic ultrasound features of pancreatic schwannoma. Endosc Ultrasound 2016; 5: 396-398
  • 8 Gkolfakis P, Crinò SF, Tziatzios G. et al. Comparative diagnostic performance of end-cutting fine-needle biopsy needles for endoscopic ultrasound tissue sampling of solid pancreatic masses: a network meta-analysis. Gastrointest Endosc 2022; DOI: 10.1016/j.gie.2022.01.019.
  • 9 Bang JY, Hebert-Magee S, Navaneethan U. et al. EUS-guided fine needle biopsy of pancreatic masses can yield true histology. Gut 2018; 67: 2081-2084
  • 10 Crinò SF, Le Grazie M, Manfrin E. et al. Randomized trial comparing fork-tip and side-fenestrated needles for EUS-guided fine-needle biopsy of solid pancreatic lesions. Gastrointest Endosc 2020; 92: 648-658
  • 11 Bang JY, Hebert-Magee S, Navaneethan U. et al. Randomized trial comparing the Franseen and Fork-tip needles for EUS-guided fine-needle biopsy sampling of solid pancreatic mass lesions. Gastrointest Endosc 2018; 87: 1432-1438
  • 12 Ashat M, Klair JS, Rooney SL. et al. Randomized controlled trial comparing the Franseen needle with the Fork-tip needle for EUS-guided fine-needle biopsy. Gastrointest Endosc 2021; 93: 140-150
  • 13 Facciorusso A, Del Prete V, Buccino VR. et al. Diagnostic yield of Franseen and Fork-Tip biopsy needles for endoscopic ultrasound-guided tissue acquisition: a meta-analysis. Endosc Int Open 2019; 7: E1221-E1230
  • 14 Mohan BP, Shakhatreh M, Garg R. et al. Comparison of Franseen and fork-tip needles for EUS-guided fine-needle biopsy of solid mass lesions: a systematic review and meta-analysis. Endosc Ultrasound 2019; 8: 382-391
  • 15 Dreyer SB, Jamieson NB, Evers L. et al. Feasibility and clinical utility of endoscopic ultrasound guided biopsy of pancreatic cancer for next-generation molecular profiling. Chin Clin Oncol 2019; 8: 16
  • 16 Gleeson FC, Kerr SE, Kipp BR. et al. Targeted next generation sequencing of endoscopic ultrasound acquired cytology from ampullary and pancreatic adenocarcinoma has the potential to aid patient stratification for optimal therapy selection. Oncotarget 2016; 7: 54526-54536
  • 17 Gleeson FC, Voss JS, Kipp BR. et al. Assessment of pancreatic neuroendocrine tumor cytologic genotype diversity to guide personalized medicine using a custom gastroenteropancreatic next-generation sequencing panel. Oncotarget 2017; 8: 93464-93475
  • 18 Rimbaş M, Crino SF, Gasbarrini A. et al. EUS-guided fine-needle tissue acquisition for solid pancreatic lesions: finally moving from fine-needle aspiration to fine-needle biopsy?. Endosc Ultrasound 2018; 7: 137-140
  • 19 Chen JY, Ding QY, Lv Y. et al. Slow-pull and different conventional suction techniques in endoscopic ultrasound-guided fine-needle aspiration of pancreatic solid lesions using 22-gauge needles. World J Gastroenterol 2016; 22: 8790-8797
  • 20 Bor R, Vasas B, Fábián A. et al. Prospective comparison of slow-pull and standard suction techniques of endoscopic ultrasound-guided fine needle aspiration in the diagnosis of solid pancreatic cancer. BMC Gastroenterol 2019; 19: 6
  • 21 Attam R, Arain MA, Bloechl SJ. et al. “Wet suction technique (WEST)”: a novel way to enhance the quality of EUS-FNA aspirate. Results of a prospective, single-blind, randomized, controlled trial using a 22-gauge needle for EUS-FNA of solid lesions.. Gastrointest Endosc 2015; 81: 1401-1407
  • 22 Capurso G, Archibugi L, Petrone MC. et al. Slow-pull compared to suction tech-nique for EUS-guided sampling of pancreatic solid lesions: a meta-analysis of randomized controlled trials. Endosc Int Open 2020; 8: E636-E643
  • 23 Wang Y, Wang RH, Ding Z. et al. Wet- versus dry-suction techniques for endoscopic ultrasound-guided fine-needle aspiration of solid lesions: a multicenter randomized controlled trial. Endoscopy 2020; 52: 995-1003
  • 24 Mendoza Ladd A, Casner N, Cherukuri SV. et al. Fine needle biopsies of solid pancreatic lesions: tissue acquisition technique and needle design do not impact specimen adequacy. Dig Dis Sci 2021; DOI: 10.1007/s10620-021-07316-4.
  • 25 Bang JY, Magee SH, Ramesh J. et al. Randomized trial comparing fanning with standard technique for endoscopic ultrasound‐guided fine‐needle aspiration of solid pancreatic mass lesions. Endoscopy 2013; 45: 445-450
  • 26 Di Leo M, Crinò SF, Bernardoni L. et al. EUS-guided core biopsies of pancreatic solid masses using a new fork-tip needle: a multicenter prospective study. Dig Liver Dis 2019; 51: 1275-1280
  • 27 Fabbri C, Luigiano C, Maimone A. et al. Endoscopic ultrasound-guided fine-needle biopsy of small solid pancreatic lesions using a 22-gauge needle with side fenestration. Surg Endosc 2015; 29: 1586-1590
  • 28 Armellini E, Manfrin E, Trisolini E. et al. Histologic retrieval rate of a newly designed side-bevelled 20G needle for EUS-guided tissue acquisition of solid pancreatic lesions. United European Gastroenterol J 2019; 7: 96-104
  • 29 Crinò SF, Di Mitri R, Nguyen NQ. et al. Endoscopic ultrasound-guided fine-needle biopsy with or without rapid on-site evaluation for diagnosis of solid pancreatic lesions: a randomized controlled non-inferiority trial. Gastroenterology 2021; 161: 899-909
  • 30 Crinò SF, Larghi A, Bernardoni L. et al. Touch imprint cytology on endoscopic ultrasound fine-needle biopsy provides comparable sample quality and diagnostic yield to standard endoscopic ultrasound fine-needle aspiration specimens in the evaluation of solid pancreatic lesions. Cytopathology 2019; 30: 179-186
  • 31 Alatawi A, Beuvon F, Grabar S. et al. Comparison of 22G reverse-beveled versus standard needle for endoscopic ultrasound-guided sampling of solid pancreatic lesions. United European Gastroenterol J 2015; 3: 343-352
  • 32 Wani S, Muthusamy VR, McGrath CM. et al. AGA White Paper: Optimizing endoscopic ultrasound-guided tissue acquisition and future directions. Clin Gastroenterol Hepatol 2018; 16: 318-327
  • 33 Pitman MB, Layfield L. The Papanicolaou Society of Cytopathology system for reporting pancreaticobiliary cytology. Switzerland: Springer International Publishing; 2015: 6
  • 34 Facciorusso A, Bajwa HS, Menon K. et al. Comparison between 22G aspiration and 22G biopsy needles for EUS-guided sampling of pancreatic lesions: a meta-analysis. Endosc Ultrasound 2020; 9: 167-174
  • 35 Facciorusso A, Sunny SP, Del Prete V. et al. Comparison between fine-needle biopsy and fine-needle aspiration for EUS-guided sampling of subepithelial lesions: a meta-analysis. Gastrointest Endosc 2020; 91: 14-22
  • 36 Machin D, Campbell MJ, Fayers P, Pinol A. Sample size tables for clinical studies (2nd edn.). Oxford: Blackwell Science; 1997
  • 37 Kahan BC. Accounting for centre-effects in multicentre trials with a binary outcome – when, why, and how?. BMC Med Res Methodol 2014; 14: 20
  • 38 Schulz KF, Altman DG, Moher D. for the CONSORT Group. CONSORT 2010 Statement: updated guidelines for reporting parallel group randomized trials. Open Med 2010; 4: 60-68
  • 39 Bang JY, Krall K, Jhala N. et al. Comparing needles and methods of endoscopic ultrasound-guided fine-needle biopsy to optimize specimen quality and diagnostic accuracy for patients with pancreatic masses in a randomized trial. Clin Gastroenterol Hepatol 2021; 19: 825-835
  • 40 Crinò SF, Conti Bellocchi MC, Bernardoni L. et al. Diagnostic yield of EUS-FNA of small (≤15 mm) solid pancreatic lesions using a 25-gauge needle. Hepatobiliary Pancreat Dis Int 2018; 17: 70-74

Corresponding author

Stefano F. Crinò, MD
Department of Medicine, Gastroenterology and Digestive Endoscopy Unit
The Pancreas Institute, University Hospital of Verona
P.le L.A. Scuro 10
37134 – Verona
Italy   

Publication History

Received: 10 April 2022

Accepted after revision: 01 August 2022

Accepted Manuscript online:
01 August 2022

Article published online:
27 September 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

  • References

  • 1 Dumonceau JM, Polkowski M, Larghi A. et al. European Society of Gastrointestinal Endoscopy. Indications, results, and clinical impact of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline. . Endoscopy 2011; 43: 897-912
  • 2 Hikichi T, Irisawa A, Bhutani MS. et al. Endoscopic ultrasound-guided fine-needle aspiration of solid pancreatic masses with rapid on-site cytological evaluation by endosonographers without attendance of cytopathologists. J Gastroenterol 2009; 44: 322-328
  • 3 Polkowski M, Jenssen C, Kaye P. et al. Technical aspects of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Technical Guideline – March 2017. Endoscopy 2017; 49: 989-1006
  • 4 Bang JY, Navaneethan U, Hasan MK. et al. Endoscopic ultrasound-guided specimen collection and evaluation techniques affect diagnostic accuracy. Clin Gastroenterol Hepatol 2018; 16: 1820-1828
  • 5 Erickson RA, Sayage-Rabie L, Beissner RS. Factors predicting the number of EUS-guided fine-needle passes for diagnosis of pancreatic malignancies. Gastrointest Endosc 2000; 51: 184-190
  • 6 Wani S. Basic techniques in endoscopic ultrasound-guided fine needle aspiration: role of a stylet and suction. Endosc Ultrasound 2014; 3: 17-21
  • 7 Crinò SF, Bernardoni L, Manfrin E. et al. Endoscopic ultrasound features of pancreatic schwannoma. Endosc Ultrasound 2016; 5: 396-398
  • 8 Gkolfakis P, Crinò SF, Tziatzios G. et al. Comparative diagnostic performance of end-cutting fine-needle biopsy needles for endoscopic ultrasound tissue sampling of solid pancreatic masses: a network meta-analysis. Gastrointest Endosc 2022; DOI: 10.1016/j.gie.2022.01.019.
  • 9 Bang JY, Hebert-Magee S, Navaneethan U. et al. EUS-guided fine needle biopsy of pancreatic masses can yield true histology. Gut 2018; 67: 2081-2084
  • 10 Crinò SF, Le Grazie M, Manfrin E. et al. Randomized trial comparing fork-tip and side-fenestrated needles for EUS-guided fine-needle biopsy of solid pancreatic lesions. Gastrointest Endosc 2020; 92: 648-658
  • 11 Bang JY, Hebert-Magee S, Navaneethan U. et al. Randomized trial comparing the Franseen and Fork-tip needles for EUS-guided fine-needle biopsy sampling of solid pancreatic mass lesions. Gastrointest Endosc 2018; 87: 1432-1438
  • 12 Ashat M, Klair JS, Rooney SL. et al. Randomized controlled trial comparing the Franseen needle with the Fork-tip needle for EUS-guided fine-needle biopsy. Gastrointest Endosc 2021; 93: 140-150
  • 13 Facciorusso A, Del Prete V, Buccino VR. et al. Diagnostic yield of Franseen and Fork-Tip biopsy needles for endoscopic ultrasound-guided tissue acquisition: a meta-analysis. Endosc Int Open 2019; 7: E1221-E1230
  • 14 Mohan BP, Shakhatreh M, Garg R. et al. Comparison of Franseen and fork-tip needles for EUS-guided fine-needle biopsy of solid mass lesions: a systematic review and meta-analysis. Endosc Ultrasound 2019; 8: 382-391
  • 15 Dreyer SB, Jamieson NB, Evers L. et al. Feasibility and clinical utility of endoscopic ultrasound guided biopsy of pancreatic cancer for next-generation molecular profiling. Chin Clin Oncol 2019; 8: 16
  • 16 Gleeson FC, Kerr SE, Kipp BR. et al. Targeted next generation sequencing of endoscopic ultrasound acquired cytology from ampullary and pancreatic adenocarcinoma has the potential to aid patient stratification for optimal therapy selection. Oncotarget 2016; 7: 54526-54536
  • 17 Gleeson FC, Voss JS, Kipp BR. et al. Assessment of pancreatic neuroendocrine tumor cytologic genotype diversity to guide personalized medicine using a custom gastroenteropancreatic next-generation sequencing panel. Oncotarget 2017; 8: 93464-93475
  • 18 Rimbaş M, Crino SF, Gasbarrini A. et al. EUS-guided fine-needle tissue acquisition for solid pancreatic lesions: finally moving from fine-needle aspiration to fine-needle biopsy?. Endosc Ultrasound 2018; 7: 137-140
  • 19 Chen JY, Ding QY, Lv Y. et al. Slow-pull and different conventional suction techniques in endoscopic ultrasound-guided fine-needle aspiration of pancreatic solid lesions using 22-gauge needles. World J Gastroenterol 2016; 22: 8790-8797
  • 20 Bor R, Vasas B, Fábián A. et al. Prospective comparison of slow-pull and standard suction techniques of endoscopic ultrasound-guided fine needle aspiration in the diagnosis of solid pancreatic cancer. BMC Gastroenterol 2019; 19: 6
  • 21 Attam R, Arain MA, Bloechl SJ. et al. “Wet suction technique (WEST)”: a novel way to enhance the quality of EUS-FNA aspirate. Results of a prospective, single-blind, randomized, controlled trial using a 22-gauge needle for EUS-FNA of solid lesions.. Gastrointest Endosc 2015; 81: 1401-1407
  • 22 Capurso G, Archibugi L, Petrone MC. et al. Slow-pull compared to suction tech-nique for EUS-guided sampling of pancreatic solid lesions: a meta-analysis of randomized controlled trials. Endosc Int Open 2020; 8: E636-E643
  • 23 Wang Y, Wang RH, Ding Z. et al. Wet- versus dry-suction techniques for endoscopic ultrasound-guided fine-needle aspiration of solid lesions: a multicenter randomized controlled trial. Endoscopy 2020; 52: 995-1003
  • 24 Mendoza Ladd A, Casner N, Cherukuri SV. et al. Fine needle biopsies of solid pancreatic lesions: tissue acquisition technique and needle design do not impact specimen adequacy. Dig Dis Sci 2021; DOI: 10.1007/s10620-021-07316-4.
  • 25 Bang JY, Magee SH, Ramesh J. et al. Randomized trial comparing fanning with standard technique for endoscopic ultrasound‐guided fine‐needle aspiration of solid pancreatic mass lesions. Endoscopy 2013; 45: 445-450
  • 26 Di Leo M, Crinò SF, Bernardoni L. et al. EUS-guided core biopsies of pancreatic solid masses using a new fork-tip needle: a multicenter prospective study. Dig Liver Dis 2019; 51: 1275-1280
  • 27 Fabbri C, Luigiano C, Maimone A. et al. Endoscopic ultrasound-guided fine-needle biopsy of small solid pancreatic lesions using a 22-gauge needle with side fenestration. Surg Endosc 2015; 29: 1586-1590
  • 28 Armellini E, Manfrin E, Trisolini E. et al. Histologic retrieval rate of a newly designed side-bevelled 20G needle for EUS-guided tissue acquisition of solid pancreatic lesions. United European Gastroenterol J 2019; 7: 96-104
  • 29 Crinò SF, Di Mitri R, Nguyen NQ. et al. Endoscopic ultrasound-guided fine-needle biopsy with or without rapid on-site evaluation for diagnosis of solid pancreatic lesions: a randomized controlled non-inferiority trial. Gastroenterology 2021; 161: 899-909
  • 30 Crinò SF, Larghi A, Bernardoni L. et al. Touch imprint cytology on endoscopic ultrasound fine-needle biopsy provides comparable sample quality and diagnostic yield to standard endoscopic ultrasound fine-needle aspiration specimens in the evaluation of solid pancreatic lesions. Cytopathology 2019; 30: 179-186
  • 31 Alatawi A, Beuvon F, Grabar S. et al. Comparison of 22G reverse-beveled versus standard needle for endoscopic ultrasound-guided sampling of solid pancreatic lesions. United European Gastroenterol J 2015; 3: 343-352
  • 32 Wani S, Muthusamy VR, McGrath CM. et al. AGA White Paper: Optimizing endoscopic ultrasound-guided tissue acquisition and future directions. Clin Gastroenterol Hepatol 2018; 16: 318-327
  • 33 Pitman MB, Layfield L. The Papanicolaou Society of Cytopathology system for reporting pancreaticobiliary cytology. Switzerland: Springer International Publishing; 2015: 6
  • 34 Facciorusso A, Bajwa HS, Menon K. et al. Comparison between 22G aspiration and 22G biopsy needles for EUS-guided sampling of pancreatic lesions: a meta-analysis. Endosc Ultrasound 2020; 9: 167-174
  • 35 Facciorusso A, Sunny SP, Del Prete V. et al. Comparison between fine-needle biopsy and fine-needle aspiration for EUS-guided sampling of subepithelial lesions: a meta-analysis. Gastrointest Endosc 2020; 91: 14-22
  • 36 Machin D, Campbell MJ, Fayers P, Pinol A. Sample size tables for clinical studies (2nd edn.). Oxford: Blackwell Science; 1997
  • 37 Kahan BC. Accounting for centre-effects in multicentre trials with a binary outcome – when, why, and how?. BMC Med Res Methodol 2014; 14: 20
  • 38 Schulz KF, Altman DG, Moher D. for the CONSORT Group. CONSORT 2010 Statement: updated guidelines for reporting parallel group randomized trials. Open Med 2010; 4: 60-68
  • 39 Bang JY, Krall K, Jhala N. et al. Comparing needles and methods of endoscopic ultrasound-guided fine-needle biopsy to optimize specimen quality and diagnostic accuracy for patients with pancreatic masses in a randomized trial. Clin Gastroenterol Hepatol 2021; 19: 825-835
  • 40 Crinò SF, Conti Bellocchi MC, Bernardoni L. et al. Diagnostic yield of EUS-FNA of small (≤15 mm) solid pancreatic lesions using a 25-gauge needle. Hepatobiliary Pancreat Dis Int 2018; 17: 70-74

Zoom Image
Fig. 1 CONSORT flow chart of the study [38]. EUS, endoscopic ultrasound.