Forward-viewing echoendoscope versus standard echoendoscope for endoscopic ultrasound-guided tissue acquisition of solid lesions: a randomized, multicenter study

• Abstract
• Introduction
• Methods
• Study design
• Patients
• EUS procedures and specimen handling
• Definition of standard reference
• Outcome parameters
• Sample size calculation
• Statistical analyses
• Results
• Study population
• Lesion identification and EUS-TA technical success rates
• Diagnostic performance and safety
• Ease of procedures
• Discussion
• References

Abstract

Background A forward-viewing linear (FVL) echoendoscope has been developed with the aim of overcoming some of the limitations of standard curved linear-array (CLA) echoendoscopes. There are no existing studies comparing the performance of the two echoendoscopes for endoscopic ultrasound-guided tissue acquisition (EUS-TA) of solid lesions other than subepithelial lesions.

Methods This was a prospective, multicenter, randomized trial with a noninferiority design comparing FVL vs. CLA echoendoscopes in patients with solid lesions of the gastrointestinal tract or adjacent organs. Primary outcomes were successful identification of the lesion and success of EUS-TA. Secondary outcomes were safety, sensitivity, specificity, and diagnostic accuracy of the two different scopes for EUS-TA.

Results 126 patients with solid lesions were randomly assigned to the CLA group (63 patients) or the FVL group (63 patients). The two groups were homogeneous with no differences in terms of needle type used, mean number of passes, and site of EUS-TA. No differences were observed between the FVL vs. CLA scopes in identification of the lesion (96.8 % vs. 98.4 %; P > 0.99) and technical success of EUS-TA (92.1 % vs. 96.8 %; P = 0.44). No adverse events occurred. Overall, diagnostic accuracy (77.8 % vs. 84.1 %), sensitivity (76.6 % vs. 84.1 %), and specificity (81.3 % vs. 84.2 %) did not differ between the two groups.

Conclusions Our results strongly suggest that the FVL echoendoscope is noninferior to the CLA scope for the detection and performance of EUS-TA in patients with solid lesions of the gastrointestinal tract and adjacent organs. In addition, the FVL scope has the same diagnostic yield, accuracy, and safety as the CLA scope.

Introduction

The introduction of the curved linear-array (CLA) echoendoscope has facilitated endoscopic ultrasound-guided tissue acquisition (EUS-TA), which has become an important tool in diagnostic algorithms for the evaluation of lesions throughout the gastrointestinal tract (GI) and adjacent organs [1] [2]. Moreover, the CLA scope is endowed with an operative working channel (at least 3.7 mm) that allows the passage of accessories larger than fine-needle aspiration (FNA) needles, and has promoted the evolution of EUS from a diagnostic into a therapeutic procedure, thus expanding the indications of EUS [3]. The CLA echoendoscope has not changed substantially since its introduction to the market: it is characterized by an oblique endoscopic view, rotated by 45° to 55° relative to the axis of the device, and the trajectory of output of any accessory device is also oblique, making it difficult to pass larger caliber instruments. Furthermore, the angle might hinder the completion of the procedure, as evidenced in the drainage of pancreatic pseudocysts [4].

Recently, a forward-viewing linear (FVL) echoendoscope has been developed with the aim of overcoming the limitations of the standard CLA scope and potentially expanding the interventional indications of EUS [5]. The FVL scope is characterized by a change in orientation of the endoscopic and ultrasonographic view from oblique to forward. This change could lead to some advantages, particularly during interventional procedures, allowing the output of accessories to be parallel to the longitudinal axis of the endoscope, thus exerting all of the force onto the tip of the accessory itself, making the procedure theoretically technically easier [4] [6] ([Fig. 1]). Moreover, although the EUS scanning angle has been substantially reduced from 180° to 90°, the change in the orientation and in the design of the tip allows the inspection of areas of the GI tract that are difficult to access using the CLA echoendoscope ([Fig. 2]) [7] [8] [9] [10] [11].

The performance of the FVL echoendoscope was initially evaluated by case reports and small case series, which highlighted the potential benefits of diagnostic sampling with the new scope in the evaluation of suspected hilar strictures [12], and pancreatic and GI lesions [8] [9] [10] [13] [14] [15] [16] [17]. Subsequently, the Catholic University group in Rome conducted two large studies, which involved more than 400 patients. In the first study [18], the EUS-guided fine-needle tissue acquisition technique was used in 121 patients for the histopathological evaluation of subepithelial lesions located throughout the GI tract. The diagnostic adequacy was 93.4 %, with a sensitivity of 92.8 % and specificity of 100 %. In the second study [19], the performance of the FVL echoendoscope for FNA of solid and cystic lesions throughout the GI tract was retrospectively evaluated in 285 patients, and an overall sensitivity of 74.7 %, specificity of 100 % for all lesions, and a technical failure rate of 2 % were reported. More recently, a Japanese group has performed a randomized comparative crossover study limited to patients with subepithelial lesions, which demonstrated no substantial difference between the CLA and FVL scopes [20]. However, no comparative data in other patient populations are available.

We conducted a large, prospective, multicenter, randomized trial with the primary aim of comparing the performance of the CLA vs. the FVL echoendoscopes for the detection and tissue acquisition of solid lesions of the GI tract and adjacent organs.

Methods

Study design

This study was a prospective, multicenter, randomized trial conducted at three European reference centers (Catholic University, Rome, Italy; University of Amsterdam, Netherlands; Erasme University Hospital, Brussels, Belgium). Patients suitable for EUS-TA were randomized to undergo examination with either the CLA or FVL scope. Randomization was performed by the endosonographer involved in the procedure using an internet randomization module. In cases of failure to identify the lesion or failure of tissue acquisition, the procedure was crossed over to the other study arm. Data were stored in each center until follow-up was concluded. All data were then sent to the Catholic University in Rome (Italy) for data analysis.

The protocol was approved by the institutional medical ethical committee at each participating institution, and written informed consent was obtained from all patients for participation in the study. The trial was registered in a publicly accessible registry.

Patients

All consecutive patients with a newly diagnosed solid lesion in the GI tract or in one of the adjacent organs who were suitable for EUS-TA were considered for enrollment.

The inclusion criteria were: 1) presence of a solid lesion in the GI tract or in one of the adjacent organs identified at abdominal ultrasound, computed tomography (CT), or magnetic resonance imaging, which needed to be sampled via EUS-TA for tissue characterization before deciding on further treatment modalities; 2) age ≥ 18 years; 3) absence of histological or cytological confirmation of malignancy; 4) informed consent obtained.

Exclusion criteria were: 1) patients with active coagulopathy that could not be corrected after administration of plasma; 2) resectable lesions for which tissue characterization was not requested by the referring physician; 3) pregnancy; 4) patients who could not give informed consent.

The investigator could decide to withdraw a patient from the study for urgent medical reasons.

EUS procedures and specimen handling

All procedures were performed with the patient in the left lateral position and under conscious sedation with midazolam and fentanyl or deep sedation.

EUS was performed using the newly available FVL scope (X GIF-UCT-160J-AL5; Olympus Medical Systems Europe, Hamburg, Germany) or the standard therapeutic CLA scopes (GF-UTC 140, GF-UTC 180). All of the EUS scopes were used with the most recent generation of Aloka alpha 10 EUS processor.

First, the endoscopist searched for the presumed lesion and, once identified, the lesion characteristics (size, echogenicity, margins, etc.) were recorded on a data collection sheet. Moreover, in cases of solid lesions of the pancreas, mediastinum, abdomen, and pelvis, the relationship of the lesion to vascular structures and surrounding organs was also investigated and reported. Tissue acquisition was performed under EUS guidance using a 19-gauge needle (Echotip Ultra; Cook Medical, Bloomington, Indiana, USA) for histology and a 22- or 25-gauge needle (Echotip Ultra; Cook Medical) for cytology. The choice of needle was left to the discretion of the endosonographer. As no onsite cytopathologist was available, for cytological specimens a minimum of three needle passes for lymph nodes and other solid lesions were performed per patient. Cytological samples were processed as directed smears [21] or were placed in Cytolit (Hologic-Cytyc Co., Marlborough, Massachusetts, USA) to perform liquid-based cytology [22]. Specimens for histological examination were placed in formalin for subsequent evaluation. In both cytological and histological sampling, the fanning technique [23] was used in association with aspiration using a 10-mL syringe.

Pictures of the identified lesion and of the needle inside the lesion were taken and stored to prove identification and puncture of the target lesion.

Endosonographers were asked to grade the ease of the procedure: 1) scope introduction; 2) lesion visualization; 3) positioning for FNA; 4) pushing the needle outside the scope working channel; 5) back and forth motion inside the lesion. A 6-point visual analog scale (VAS) was used, from 1 (very easy) to 6 (impossible).

Adverse events were divided into procedural and post-procedural (within 72 hours), and were recorded and followed until they had abated, or until a stable situation had been reached. A phone call was made to all patients 3 days after the procedure to check for delayed adverse events.

Definition of standard reference

A cytological or histological EUS-TA specimen that was positive for malignancy was considered as a positive result. Atypical or suspicious, as well as benign cytological specimens were considered as negative. Nondiagnostic specimens were considered as false negatives, regardless of the definitive diagnosis, in order to represent the worst-case scenario. For patients with benign or negative EUS-TA specimens, the presence or exclusion of malignancy was based on the following criteria: the histopathological examination of the surgically resected specimen; the results of other diagnostic investigation, such as CT-guided and/or laparoscopic biopsy indicating the presence of malignancy; and/or the long-term clinical follow-up of at least 1 year, including imaging studies, as used in other clinical studies. For this purpose, patients who had negative results were evaluated for a minimum of 1 year. This evaluation included periodic chest/abdominal CT in order to assess the growth of the lesion and repeat sampling if needed. Further radiological studies were conducted if substantial growth of the lesion was identified.

Vascular involvement by the lesion was considered present if any of the following was noted: loss of the normal hyperechoic interface between tumor and vessel for at least 5 mm (adherence); irregular tumor and vessel interface; tumor within vessel lumen (invasion); vessel surrounded by the tumor (encasement).

Outcome parameters

The primary end points of interest were the successful identification of the lesion and the success of EUS-TA by EUS image confirming the needle inside the lesion.

Secondary end points were performance of the endoscopes, in terms of sensitivity, specificity, and diagnostic accuracy of EUS-TA, diagnostic yield (i. e. the proportion of specimens judged as adequate for pathological examination), and procedure-related adverse events.

Sample size calculation

To calculate the study size, we considered as primary end point the rate of successful FNA, defined by an EUS image confirming the needle inside the lesion, as this outcome reasonably also included the successful identification of the lesion. For the primary end point, a one-tailed noninferiority design was used to compare CLA and FVL echoendoscopes. Using an α = 0.05 and 1 – β = 0.8, and assuming CLA results of successful tissue acquisition in at least 95 % of cases and rejecting FVL as inferior at a success rate of 85 % (margin of equivalence of 10 %), a sample size of at least 59 patients in each group was determined. To compensate for potential withdrawal of 5 % of the patients (e. g. due to misdiagnosis), the desired number of cases was calculated to be 124 patients in total.

Statistical analyses

The analyses were performed in accordance with the intention-to-treat principle. Continuous variables were reported as mean (SD), count variables were reported as median and interquartile range (IQR), and categorical variables were summarized as proportions. Comparisons between the two study groups were performed using the unpaired t test or the Mann-Whitney U test, and the chi-squared test or Fisher’s exact test, as appropriate. Primary outcomes (i. e. identification of the lesion and EUS-TA technical success) were reported with exact binomial 95 % confidence interval (CI) in order to test for the noninferiority hypothesis. Overall accuracy, sensitivity, specificity, positive likelihood ratio, and negative likelihood ratio were calculated, along with binomial 95 %CIs. For the purpose of this study, definitive diagnoses were divided into malignant and benign lesions. Samples that were inadequate for pathological evaluation were considered as false-negative cases. Statistical analyses were performed using R version 3.4.2 for Mac [24].

Results

Study population

At the time of the study, only a single prototype of the FVL echoendoscope was available. Thus, each center received and kept the FVL scope for a 6-month period starting June 2012 to December 2013, with the goal of enrolling at least a third of the calculated sample size at each center. With the addition of the follow-up period, the study ended in December 2014. During the study period, a total of 655 consecutive patients were screened for participation in the study. A total of 529 patients were excluded, leaving 126 patients to be randomized to either the CLA group (63 patients) or the FVL group (63 patients) ([Fig. 3]).

The groups were homogeneous according to age and sex distribution, as well as lesion site, type, mean diameter, and infiltration rate of main locoregional vascular structures. Details are summarized in [Table 1].

Lesion identification and EUS-TA technical success rates

The two groups did not differ statistically in terms of needle type used, mean number of passes, and site of EUS-TA. The identification rates exceeded 95 % in both groups (FVL vs. CLA: 96.8 % vs. 98.4 %; P > 0.99) with no statistical difference. The FVL scope failed to visualize two lesions, and the CLA scope did not find one lesion. EUS-TA was technically successful in 58 procedures in the FVL group (92.1 %) and 61 procedures in the CLA group (96.8 %), again without significant difference (P = 0.44). Crossover to the CLA group enabled detection of the two missing lesions and tissue was obtained from one of them. Crossover to the FVL group visualized the missing lesion, but tissue acquisition was not possible in one of the two lesions not biopsied by the CLA. The same diagnostic yield was reported in both groups (FVL vs. CLA: 84.1 % vs. 84.1 %; P > 0.99). More details are reported in [Table 2]. Representative images of EUS-TA of pancreatic lesions performed with each scope are shown in [Fig. 4].

Diagnostic performance and safety

Diagnostic accuracy (FVL vs. CLA: 77.8 % vs. 84.1 %), sensitivity (76.6 % vs. 84.1 %), and specificity (81.3 % vs. 84.2 %) did not differ significantly between the two study groups ([Table 3], [Table 4]).

No immediate or delayed EUS-related adverse events were reported in the two study groups.

Ease of procedures

The ease of the EUS-TA procedures was analyzed from the questionnaire completed by endosonographers. As detailed in [Table 5], the two study groups did not differ significantly in any of the main items; in particular, median (IQR) VAS scores for ease of scope introduction was 1 (1 – 2) vs. 1 (1 – 2) with the FVL and CLA scopes, respectively. The experience of tissue acquisition was judged to be satisfactory in more than 80 % of the procedures using the FVL scope and in more than 90 % of patients undergoing the procedure with the CLA scope.

Discussion

We performed a multicenter randomized study to directly compare the performance of the FVL and the CLA echoendoscopes in EUS-TA of solid lesions throughout the GI tract and adjacent organs in a large patient population. Overall, the two scopes did not show any significant difference in any of the outcome measures (i. e. identification of solid lesions, technical success of EUS-TA, diagnostic yield and accuracy, and ease of use).

The performance of the FVL scope was first compared with a CLA scope for transgastric drainage of pancreatic pseudocysts [25], without any advantages of the forward-viewing design over the standard CLA device. Subsequently, after a series of small studies and case reports [8] [9] [10] [12] [13] [14] [15] [16] [17] [18], two large, single-center studies were published evaluating the performance of the FVL echoendoscope in patients with solid and cystic lesions throughout the GI tract and in patients with subepithelial lesions [18] [19]. Both studies showed good performance for the FVL scope. The prospective study on 121 patients with subepithelial lesions showed that tissue samples for histopathological examination were successfully obtained in 93.4 % of patients, with a sensitivity of 92.8 % and specificity of 100 %, allowing immunohistochemical studies to differentiate neoplastic from non-neoplastic lesions in all patients with available tissue [18].

This impressively high diagnostic accuracy found in patients with subepithelial lesions prompted a Japanese group to perform a randomized, crossover, comparative study in 41 patients who had subepithelial lesions and underwent sampling by both the FVL and the CLA scopes, with diagnostic yield as the primary outcome [20]. A 19-gauge needle was used in all cases, and was then changed to a 22- or a 25-gauge needle, if required. Rates of histological diagnosis did not differ between the two echoendoscopes (80.5 % for FVL vs. 73.2 % for CLA). However, the median tissue sample area obtained with the FVL scope in GI stromal tumors was significantly larger than that obtained with the CLA scope (2.46 vs. 1.00 mm²; P = 0.046) and the mean procedural time was significantly shorter when the FVL scope was used (21 vs. 27 minutes; P = 0.01). Moreover, although tissue sampling using the 19-gauge needle was equally successful with both echoendoscopes (FVL 70.7 % vs. CLA 58.5 %), the time required to perform the procedure with this needle size was significantly shorter when the FVL device was used (17 vs. 25 minutes; P = 0.004) [20].

To date, however, no data directly comparing the two scopes in the performance of EUS-TA for solid lesions other than subepithelial lesions have been available. To address this gap, we performed a multicenter, randomized, comparative study to evaluate patients with solid lesions of the GI tract and adjacent organs. Our hypothesis was that the performance of the FVL echoendoscope was not inferior to the standard CLA scopes, and we used this assumption to calculate the number of patients needed in the study. In contrast to the Japanese study [20], in which patients underwent sampling with both scopes, in our study, patients were randomly assigned to undergo sampling using either the FVL or the CLA scope, while crossover was permitted only in cases of failure.

Overall, the results of our study, which showed no differences between the two scopes in terms of identifying solid lesions, technical success of EUS-TA, diagnostic yield and accuracy, and ease of use, fulfil completely our hypothesis that the FVL echoendoscope is comparable to the CLA scope in patients with solid lesions throughout the GI tract and adjacent organs. These results were obtained despite the fact that in almost half of the patients (46.6 %), EUS-TA was performed from the duodenum, and in 8/19 (42.1 %) transduodenal FVL cases, puncture was done from the second duodenal portion. In our previous study in a similar patient population [19], all failures occurred when the procedure was performed transduodenally and an overall greater difficulty was observed in performing tissue acquisition from the duodenum with the FVL scope, leading us to hypothesize that the reasons for these failures could be due to a combination of several factors, such as: 1) the narrow scanning range; 2) the frontal exit of the needle; 3) the absence of an elevator to obtain the deflection of the needle that may be required to puncture a lesion identified from the second duodenal portion.

Based on the results we obtained, it is possible to speculate that the FVL echoendoscope can expand the EUS armamentarium and be used in parallel with the CLA scope, not only to inspect and perform EUS-TA in areas of the GI tract that are difficult to access with the CLA scope [7] [8] [9] [10] [11], but also for tissue acquisition of solid lesions throughout the GI tract and adjacent organs. Moreover, further improvement of some functions, such as the development of a blocker at the end of the working channel to guarantee guidewire stability during accessory exchange, has the potential to further expand the role of the FVL device for interventional EUS [26], which is a field in extraordinary expansion. If these changes are made, EUS using the FVL echoendoscope should become part of the EUS armamentarium in tertiary referral centers.

Our study has some strengths and limitations. The main strength is the study design, which limited possible bias. The selection criteria allowed inclusion of patients with different types of lesions throughout the GI tract, thus increasing the external validity of our findings. However, the small number of lesions other than pancreatic masses included in our study did not allow us to draw definitive conclusions on the safety and efficacy of the FVL echoendoscope for these types of lesions. Furthermore, the study was not designed to identify anatomic areas or clinical scenarios in which the FVL scope may offer advantages over standard scopes. The choice of needle was at the discretion of the echoendoscopist and this may have influenced the higher number of 19-gauge needles used with the FVL device compared with the CLA scope (61.9 % vs. 49.2 %). Only tertiary referral centers with previous experience in the use of the FVL scope were included; therefore, similar outcomes might not be replicated outside of this setting, at least during the learning curve, which is, in our view, very fast. Moreover, echoendoscopists were not blinded to the scope used for the procedure. Finally, only solid mass lesions were sampled; therefore, further studies are needed to ascertain the performance of the FVL device in cystic lesions.

In conclusion, our study strongly indicates that the FVL echoendoscope is noninferior to the standard CLA scope in identification and performance of tissue acquisition of solid lesions throughout the GI tract and adjacent organs, with the same diagnostic yield and accuracy, and safety as the CLA scope. Improvement of some functions and further implementation in the echoendoscope design may render it a very useful tool in the EUS armamentarium.

Competing interests

Prof. Fockens is a consultant for Olympus Medical. Prof. Deviere has received research support for IRB-approved studies from Olympus Medical. Prof. Costamagna is a consultant for Olympus Medical and has received research grants from Olympus Medical.

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Corresponding author

• References

• 1 Eloubeidi MA, Varadarajulu S, Desai S. et al. A prospective evaluation of an algorithm incorporating routine preoperative endoscopic ultrasound-guided fine needle aspiration in suspected pancreatic cancer. J Gastrointest Surg 2007; 11: 813-819
  CrossrefPubMedSearch in Google Scholar
• 2 Erickson RA. EUS-guided FNA. Gastrointest Endosc 2004; 60: 267-279
  CrossrefPubMedSearch in Google Scholar
• 3 Fuccio L, Attili F, Vanella G. et al. Interventional endoscopic ultrasonography. Curr Treat Options Gastroenterol 2014; 12: 183-210
  CrossrefPubMedSearch in Google Scholar
• 4 Voermans RP, Eisendrath P, Bruno MJ. et al. Initial evaluation of a novel prototype forward-viewing US endoscope in transmural drainage of pancreatic pseudocysts (with videos). Gastrointest Endosc 2007; 66: 1013-1017
  CrossrefPubMedSearch in Google Scholar
• 5 Binmoeller KF. Optimizing interventional EUS: the echoendoscope in evolution. Gastrointest Endosc 2007; 66: 917-919
  CrossrefPubMedSearch in Google Scholar
• 6 Trevino JM, Varadarajulu S. Initial experience with the prototype forward-viewing echoendoscope for therapeutic interventions other than pancreatic pseudocyst drainage (with videos). Gastrointest Endosc 2009; 69: 361-365
  CrossrefPubMedSearch in Google Scholar
• 7 De Lusong MA, Shah JN, Soetikno R. et al. Treatment of a completely obstructed colonic anastomotic stricture by using a prototype forward-array echoendoscope and facilitated by SpyGlass (with videos). Gastrointest Endosc 2008; 68: 988-992
  CrossrefPubMedSearch in Google Scholar
• 8 Uchida N, Galasso D, Seerden TC. et al. EUS-FNA of extracolonic lesions by using the forward-viewing linear echoendoscope. Gastrointest Endosc 2010; 72: 1321-1323
  CrossrefPubMedSearch in Google Scholar
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  Thieme ConnectPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
• 14 Fusaroli P, Cortecchia S, Caletti G. EUS-FNA using a forward-view echoendoscope in difficult cases. J Gastrointest Liver Dis 2011; 20: 216-217
  PubMedSearch in Google Scholar
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  Thieme ConnectPubMedSearch in Google Scholar
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