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III BRAZILIAN CONSENSUS STATEMENT ON ENDOSCOPIC ULTRASOUND

III Consenso brasileiro sobre ultrassonografia endoscópica

ABSTRACT

Background:

In the past decades, endoscopic ultrasound has developed from a diagnostic tool to a platform for many therapeutic interventions. Various technological advancements have emerged since the last Brazilian Consensus, demanding a review and update of the recommendations based on the best scientific evidence.

Methods:

A group of 32 renowned echoendoscopists selected eight relevant topics to be discussed to generate clinical questions. After that, a literature review was conducted to answer these questions based on the most updated evidence.

Results:

Thirty-three statements were formulated and voted on by the experts to reach a consensus. The Oxford System was used to grade the level of evidence.

Conclusion:

There is mo­derate evidence to support that the needle shape, gauge, or aspiration technique does not influence the yield of endoscopic ultrasound (EUS)-guided tissue sampling of pancreatic solid lesions. There is moderate evidence to support using EUS-TTNB of the cyst wall to differentiate between mucinous and non-mucinous cystic neoplasms. There is little evidence to support the EUS-guided treatment of gastric varices. There is a high level of evidence to support that EUS-guided biliary drainage and ERCP present similar outcomes in patients with distal malignant biliary obstruction. There is a high level of evidence for using EUS to diagnose neoplastic pancreatic cysts and detect necrosis before indicating drainage. There is moderate evidence to support EUS-GE over duodenal stent for malignant gastric outlet obstruction in patients with a life expectancy higher than 2 months. There is a high level of evidence to support the use of RFA in treating both functioning and non-functioning types of NET.

Keywords:
Echoendoscopy; endoscopy; endoscopic ultrasound; therapeutic endoscopy; consensus

RESUMO

Contexto:

Nas últimas décadas, a ecoendoscopia evoluiu de uma ferramenta diagnóstica para uma plataforma para diversas intervenções terapêuticas. Vários avanços tecnológicos surgiram desde o último Consenso Brasileiro, demandando uma revisão e atualização das recomendações baseadas nas melhores evidências científicas.

Métodos:

Um grupo de 32 ecoendoscopistas renomados selecionou oito tópicos relevantes para serem discutidos a fim de gerar questões clínicas. Em seguida, foi realizada uma revisão da literatura para responder a essas perguntas com base nas evidências mais atualizadas.

Resultados:

Trinta e três tópicos foram formulados e votados pelos especialistas para alcançar um consenso. O Sistema de Oxford foi utilizado para classificar o nível de evidência.

Conclusão:

Há evidências moderadas para sustentar que a forma da agulha, calibre ou técnica de aspiração não influenciam no rendimento da amostragem tecidual guiada por ultrassom endoscópico (USE) de lesões sólidas pancreáticas. Há evidências moderadas para sustentar o uso da biópsia transcutânea guiada por USE da parede cística para diferenciar entre neoplasias císticas mucinosas e não mucinosas. Existem poucas evidências para apoiar o tratamento guiado por USE de varizes gástricas. Há um alto nível de evidência para sustentar que a drenagem biliar guiada por USE e a CPRE apresentam resultados semelhantes em pacientes com obstrução biliar maligna distal. Há um alto nível de evidência para o uso da USE no diagnóstico de cistos pancreáticos neoplásicos e na detecção de necrose antes de indicar a drenagem. Há evidências moderadas para sustentar a preferência pela gastroenterostomia guiada por USE em relação ao stent duodenal para obstrução maligna da saída gástrica em pacientes com expectativa de vida superior a 2 meses. Há um alto nível de evidência para sustentar o uso da ablação por radiofrequência no tratamento de ambos os tipos, funcionantes e não funcionantes, de tumores neuroendócrinos.

Palavras-chave:
Ecoendoscopia; endoscopia; ultrassom endoscópico; endoscopia terapêutica; consenso

HIGHLIGHTS

•Since its inception in the 1980s, endoscopic ultrasound has increased relevance and usefulness in clinical practice.

•Endoscopic ultrasound has evolved from solely diagnostic imaging to a valuable method for tissue sampling and therapeutic procedures, such as drainage of pancreatic fluid collections and creating gastrointestinal anastomoses under EUS guidance.

•Given the rapid advancements in EUS and new devices, an update to the last Consensus must include recent developments.

•Experts evaluated and discussed the best evidence on EUS-guided procedures and devices for tissue sampling, pancreatic and liver disease management, and biliary drainage.

INTRODUCTION

Since its inception in the 80s11. Tio TL, Tytgat GN. Endoscopic ultrasonography of an arteriovenous malformation in a gastric polyp. Endoscopy. 1986;18:156-8., endoscopic ultrasound (EUS) has earned increasing relevance and usefulness in clinical practice. Initially, it has developed from a solely diagnostic imaging tool to a valuable method for tissue sampling of subepithelial lesions (SEL) in the gastrointestinal (GI) tract and pancreatobiliary structures with the advent of linear array echoendoscopes and EUS-guided fine-needles. Later, various devices and techniques emerged and allowed the performance of a series of therapeutic EUS procedures, such as EUS-guided drainage of pancreatic fluid collections (PFC), EUS techniques for biliary tract drainage, and the creation of GI tract anastomosis with EUS guidance.

Two previous Brazilian Consensus on EUS have been published22. Maluf-Filho F, Dotti CM, Farias AQ, Kupski C, Chaves DM, Artifon E, et al. I Consenso Brasileiro de Ecoendoscopia [I Brazilian Consensus of endoscopic ultrasonography]. Arq Gastroenterol. 2007;44:353-8.,33. Maluf-Filho F, de Oliveira JF, Mendonça EQ, Carbonari A, Maciente BA, Salomão BC, et al. II Brazilian consensus statement on endoscopic ultrasonography. Endosc Ultrasound. 2017;6:359-68., addressing the most relevant subjects in EUS practice and gathering the best available evidence to that date. In 2017, the second Brazilian Consensus33. Maluf-Filho F, de Oliveira JF, Mendonça EQ, Carbonari A, Maciente BA, Salomão BC, et al. II Brazilian consensus statement on endoscopic ultrasonography. Endosc Ultrasound. 2017;6:359-68. concluded that there was a high level of evidence to support EUS-guided biopsy for SELs in the GI tract, EUS for the staging of non-small cell lung cancer, and equivalence of unilateral or bilateral EUS-guided celiac neurolysis. However, regarding the best needle or technique of EUS-guided tissue sampling in pancreatic lesions, comparison of EUS-guided biliary drainage (EUS-BD) techniques with percutaneous drainage, the definition of whether plastic or metallic stents are preferred in EUS-guided PFC drainage, and the EUS-guided treatment of gastric varices, there was still a lack of high-quality evidence and much more research to be conducted in the next few years.

Considering the considerable evolution of EUS and the rapid progression in technical advances, an update of the last Consensus is required to cover this new evidence, focusing on EUS interventions and devices that have arisen since that report.

METHODS

A group of 32 national experts in endosonography, members of the Nucleus of Endoscopic Ultrasound of the Brazilian Society of Digestive Endoscopy (SOBED), held a series of online meetings to select and discuss the topics based on clinical relevance and recent advances in the field. A total of eight subjects were proposed, including tissue acquisition in SELs of the GI tract, EUS-guided tissue sampling of pancreatic solid lesions (PSL), novel devices for EUS-guided tissue sampling in pancreatic cystic lesions (PCL), EUS in the management of liver diseases and portal hypertension, EUS-BD, EUS-guided management of PFC, EUS-guided gastroenterostomy (EUS-GE), EUS-guided radiofrequency ablation (RFA) of pancreatic neoplasms.

Further issues regarding these topics were debated in additional online meetings to generate suggestions before the clinical questions were generated. After a uniform division, the experts were designated to respond to these questions based on a literature review to raise the best scientific data available and measure the level of evidence according to the Oxford System (Table 1).

TABLE 1
Level of scientific evidence according to the type of study.

After that, a document with thirty-three statements was formulated and provided to the experts in EUS distributed throughout the Brazilian territory. They should vote individually, through a virtual form, in agreement or disagreement with each recommendation.

Consensus was achieved if at least 70% of the voting participants declared to agree with the recommendation. Four of the organizers (VLO, AMB, RRPP, and GOL) prepared a final draft that was forwarded to all the invited members for approval. After all authors approved the final manuscript, it was submitted for publication.

RESULTS

Techniques for tissue acquisition in subepithelial lesions of the GI tract

For SELs of the GI tract larger than 20 mm, EUS-fine-needle biopsy (FNB) has a higher diagnostic yield than EUS-fine-needle aspiration (FNA).

•Recommendation: B - 100% vote; evidence level 2c.

Mucosal incision-assisted biopsy (MIAB) is the preferred method for histopathological diagnosis in SELs of the GI tract smaller than 20 mm.

No agreement - 43.3% vote; evidence level 2b.

DISCUSSION

EUS is currently the preferred diagnostic tool for characterizing SELs in the GI tract. It accurately differentiates if the lesion is intramural or corresponds to an extrinsic compression and evaluates echographic features, such as the layer of origin, size, and echogenicity44. Rösch T, Kapfer B, Will U, Baronius W, Strobel M, Lorenz R, et al. Endoscopic ultrasonography. Accuracy of endoscopic ultrasonography in upper gastrointestinal submucosal lesions: a prospective multicenter study. Scand J Gastroenterol. 2002;37:856-62.. However, the imaging features are sometimes not enough to determine the exact type of lesion, requiring tissue acquisition for diagnostic confirmation55. Kim SY, Shim KN, Lee JH, Lim JY, Kim TO, Choe AR, et al. Comparison of the Diagnostic Ability of Endoscopic Ultrasonography and Abdominopelvic Computed Tomography in the Diagnosis of Gastric Subepithelial Tumors. Clin Endosc. 2019;52:565-73.,66. Karaca C, Turner BG, Cizginer S, Forcione D, Brugge W. Accuracy of EUS in the evaluation of small gastric subepithelial lesions. Gastrointest Endosc. 2010;71:722-7.. This is especially relevant for lesions with malignant potential, notably hypoechogenic lesions originating from the fourth layer, when GIST is a strong possibility, and histologic diagnosis could modify the management33. Maluf-Filho F, de Oliveira JF, Mendonça EQ, Carbonari A, Maciente BA, Salomão BC, et al. II Brazilian consensus statement on endoscopic ultrasonography. Endosc Ultrasound. 2017;6:359-68.,77. Sharzehi K, Sethi A, Savides T. AGA Clinical Practice Update on Management of Subepithelial Lesions Encountered During Routine Endoscopy: Expert Review. Clin Gastroenterol Hepatol. 2022;20:2435-43.e4.,88. Chong CC, Pittayanon R, Pausawasdi N, Bhatia V, Okuno N, Tang RS, et al. Consensus statements on endoscopic ultrasound-guided tissue acquisition. Guidelines from the Asian Endoscopic Ultrasound Group. Dig Endosc. 2024;36:871-83. doi: 10.1111/den.14768.
https://doi.org/10.1111/den.14768...
.

For gastric GISTs smaller than 20 mm, there is a very low incidence of metastasis99. He Z, Sun C, Zheng Z, Yu Q, Wang T, Chen X, et al. Endoscopic submucosal dissection of large gastrointestinal stromal tumors in the esophagus and stomach. J Gastroenterol Hepatol. 2013;28:262-7.. Thus, either surveillance or tissue sampling are accepted decisions1010. ESMO/European Sarcoma Network Working Group. Gastrointestinal stromal tumours: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2014;25(Suppl 3):iii21-6. Erratum in: Ann Oncol. 2015;26(Suppl 5):174-7.

11. Nishida T, Hirota S, Yanagisawa A, Sugino Y, Minami M, Yamamura Y, et al. Clinical practice guidelines for gastrointestinal stromal tumor (GIST) in Japan: English version. Int J Clin Oncol. 2008;13:416-30.
-1212. von Mehren M, Kane JM, Bui MM, Choy E, Connelly M, Dry S, et al. NCCN Guidelines Insights: Soft Tissue Sarcoma, Version 1.2021. J Natl Compr Canc Netw. 2020;18:1604-12.. On the other hand, tissue sampling is necessary for SELs of the GI tract larger than 20 mm. Therefore, EUS-FNB has higher diagnostic accuracy than EUS-FNA in this scenario88. Chong CC, Pittayanon R, Pausawasdi N, Bhatia V, Okuno N, Tang RS, et al. Consensus statements on endoscopic ultrasound-guided tissue acquisition. Guidelines from the Asian Endoscopic Ultrasound Group. Dig Endosc. 2024;36:871-83. doi: 10.1111/den.14768.
https://doi.org/10.1111/den.14768...
,1313. Deprez PH, Moons LMG, OʼToole D, Gincul R, Seicean A, Pimentel-Nunes P, et al. Endoscopic management of subepithelial lesions including neuroendocrine neoplasms: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2022;54:412-29.. A meta-analysis of 10 studies with 669 patients demonstrated the superiority of EUS-FNB over EUS-FNA in all diagnostic outcomes, including satisfactory tissue sampling (94.9% x 80.6%), optimal histologic core procurement rate (89.7 x 65%), diagnostic accuracy, and number of passes needed to obtain diagnostic samples1414. Facciorusso A, Sunny SP, Del Prete V, Antonino M, Muscatiello N. 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.e2.,1515. Kuraoka N, Hashimoto S, Matsui S, Terai S. Effectiveness of EUS-Guided Fine-Needle Biopsy versus EUS-Guided Fine-Needle Aspiration: A Retrospective Analysis. Diagnostics (Basel). 2021;11:965.. This higher efficacy of EUS-FNB is reinforced by two recent extensive multicentric retrospective studies1616. Trindade AJ, Benias PC, Alshelleh M, Bazarbashi AN, Tharian B, Inamdar S, et al. Fine-needle biopsy is superior to fine-needle aspiration of suspected gastrointestinal stromal tumors: a large multicenter study. Endosc Int Open. 2019;7:E931-E936.,1717. de Moura DTH, McCarty TR, Jirapinyo P, Ribeiro IB, Flumignan VK, Najdawai F, et al. EUS-guided fine-needle biopsy sampling versus FNA in the diagnosis of subepithelial lesions: a large multicenter study. Gastrointest Endosc. 2020;92:108-119.e3..

Regarding SELs with less than 20 mm, ESGE recommends that MIAB be the first choice to obtain tissue diagnosis1313. Deprez PH, Moons LMG, OʼToole D, Gincul R, Seicean A, Pimentel-Nunes P, et al. Endoscopic management of subepithelial lesions including neuroendocrine neoplasms: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2022;54:412-29., considering the lower diagnostic yield of EUS-FNB in three randomized controlled trials1818. Sanaei O, Fernández-Esparrach G, De La Serna-Higuera C, Carrara S, Kumbhari V, El Zein MH, et al. EUS-guided 22-gauge fine needle biopsy versus single-incision with needle knife for the diagnosis of upper gastrointestinal subepithelial lesions: a randomized controlled trial. Endosc Int Open. 2020;8:E266-E273.

19. Osoegawa T, Minoda Y, Ihara E, Komori K, Aso A, Goto A, et al. Mucosal incision-assisted biopsy versus endoscopic ultrasound-guided fine-needle aspiration with a rapid on-site evaluation for gastric subepithelial lesions: A randomized cross-over study. Dig Endosc. 2019;31:413-21.
-2020. Zoundjiekpon V, Falt P, Fojtik P, Kundratova E, Mikolajek O, Hanousek M, et al. Endosonography-Guided Fine-Needle Aspiration versus “Key-Hole Biopsy” in the diagnostics of upper gastrointestinal subepithelial tumors. A prospective randomized interventional study. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2020;164:63-70.. Nevertheless, the risk of complications (i.e., bleeding) of these techniques (unroofing, submucosal tunneling) must be considered, and - can be performed prior to a most invasive approach.

EUS-guided tissue sampling of pancreatic solid lesions

EUS-guided puncture of PSL is indicated:

-In surgically resectable lesions, if a diagnosis other than adenocarcinoma is suspected (neuroendocrine tumor, pancreatic metastasis, lymphoma, autoimmune pancreatitis).

- In borderline/locally advanced lesions for referral to neoadjuvant oncologic treatment or complete staging if resectability is doubtful.

- In unresectable lesions to guide oncological treatment and for genetic evaluation.

•Recommendation: A - 96.6% vote; evidence level 2a.

There is no difference in the diagnostic yield of EUS-FNA and EUS-FNB for PSL.

•Recommendation: A - 83.3% vote; evidence level 2a.

There is no superiority among the EUS-guided fine-needle techniques (wet suction, aspiration, slow pull) for PSL.

•Recommendation: B - 100% vote; evidence level 2b.

There is no definition regarding the ideal caliper of EUS-fine-needle for the puncture of PSL.

•Recommendation: B - 90% vote; evidence level 2b.

DISCUSSION

EUS-guided tissue acquisition in PSL is indicated whenever the accurate diagnosis is uncertain or histologic confirmation is mandatory prior to surgical or systemic treatment88. Chong CC, Pittayanon R, Pausawasdi N, Bhatia V, Okuno N, Tang RS, et al. Consensus statements on endoscopic ultrasound-guided tissue acquisition. Guidelines from the Asian Endoscopic Ultrasound Group. Dig Endosc. 2024;36:871-83. doi: 10.1111/den.14768.
https://doi.org/10.1111/den.14768...
,2121. Dumonceau JM, Deprez PH, Jenssen C, Iglesias-Garcia J, Larghi A, Vanbiervliet G, et al. Indications, results, and clinical impact of endoscopic ultrasound (EUS)-guided sampling in gastroenterology: European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline - Updated January 2017. Endoscopy. 2017;49:695-714.. Since the last Brazilian Consensus, the EUS-fine needles have evolved technologically, from the standard EUS-FNA needles to the development of different EUS-FNB needles. Different types of FNB needles were developed, and research was conducted to compare their diagnostic outcomes with their different tip designs, including side-bevel needles, crown-tip needles, and fork-tip needles, among others. Both EUS-FNA and EUS-FNB needles have similar high diagnostic accuracy for PSL2222. Bang JY, Hawes R, Varadarajulu S. A meta-analysis comparing ProCore and standard fine-needle aspiration needles for endoscopic ultrasound-guided tissue acquisition. Endoscopy. 2016;48:339-49.

23. Tian L, Tang AL, Zhang L, Liu XW, Li JB, Wang F, et al. Evaluation of 22G fine-needle aspiration (FNA) versus fine-needle biopsy (FNB) for endoscopic ultrasound-guided sampling of pancreatic lesions: a prospective comparison study. Surg Endosc. 2018;32:3533-9.
-2424. Pouw RE, Barret M, Biermann K, Bisschops R, Czakó L, Gecse KB, et al. Endoscopic tissue sampling - Part 1: Upper gastrointestinal and hepatopancreatobiliary tracts. European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2021;53:1174-88., even though EUS-FNB needles have a better yield of histological sampling, providing better tissue core rate and higher diagnostic adequacy with the need for fewer needle passes2525. van Riet PA, Erler NS, Bruno MJ, Cahen DL. Comparison of fine-needle aspiration and fine-needle biopsy devices for endoscopic ultrasound-guided sampling of solid lesions: a systemic review and meta-analysis. Endoscopy. 2021;53:411-23.

26. Wang J, Zhao S, Chen Y, Jia R, Zhang X. Endoscopic ultrasound guided fine needle aspiration versus endoscopic ultrasound guided fine needle biopsy in sampling pancreatic masses: A meta-analysis. Medicine (Baltimore). 2017;96:e7452.

27. Cheng B, Zhang Y, Chen Q, Sun B, Deng Z, Shan H, et al. Analysis of Fine-Needle Biopsy vs Fine-Needle Aspiration in Diagnosis of Pancreatic and Abdominal Masses: A Prospective, Multicenter, Randomized Controlled Trial. Clin Gastroenterol Hepatol. 2018;16:1314-21.
-2828. Asokkumar R, Yung Ka C, Loh T, Kah Ling L, Gek San T, Ying H, et al. Comparison of tissue and molecular yield between fine-needle biopsy (FNB) and fine-needle aspiration (FNA): a randomized study. Endosc Int Open. 2019;7:E955-E963.. This is especially valuable when histological specimens are required for molecular tests or rapid on-site evaluation (ROSE) is unavailable2424. Pouw RE, Barret M, Biermann K, Bisschops R, Czakó L, Gecse KB, et al. Endoscopic tissue sampling - Part 1: Upper gastrointestinal and hepatopancreatobiliary tracts. European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy. 2021;53:1174-88.,2828. Asokkumar R, Yung Ka C, Loh T, Kah Ling L, Gek San T, Ying H, et al. Comparison of tissue and molecular yield between fine-needle biopsy (FNB) and fine-needle aspiration (FNA): a randomized study. Endosc Int Open. 2019;7:E955-E963.,2929. Kong F, Zhu J, Kong X, Sun T, Deng X, Du Y, et al. Rapid On-Site Evaluation Does Not Improve Endoscopic Ultrasound-Guided Fine Needle Aspiration Adequacy in Pancreatic Masses: A Meta-Analysis and Systematic Review. PLoS One. 2016;11:e0163056..

Regarding the technical aspects of EUS-guided puncture, the literature is similar among the suction methods: stylet slow pull, wet suction, or standard aspiration suction3030. Polkowski M, Jenssen C, Kaye P, Carrara S, Deprez P, Gines A, 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.

31. Kin T, Katanuma A, Yane K, Takahashi K, Osanai M, Takaki R, et al. Diagnostic ability of EUS-FNA for pancreatic solid lesions with conventional 22-gauge needle using the slow pull technique: a prospective study. Scand J Gastroenterol. 2015;50:900-7.

32. Jani BS, Rzouq F, Saligram S, Lim D, Rastogi A, Bonino J, et al. Endoscopic Ultrasound-Guided Fine-Needle Aspiration of Pancreatic Lesions: A Systematic Review of Technical and Procedural Variables. N Am J Med Sci. 2016;8:1-11.
-3333. Attam R, Arain MA, Bloechl SJ, Trikudanathan G, Munigala S, Bakman Y, 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;81:1401-7.. However, the fanning technique reduces the number of passes by changing the needle direction. The ideal EUS-needle caliper has yet to be defined because there is no proven difference among the needles’ diameters3434. Carrara S, Anderloni A, Jovani M, Di Tommaso L, Rahal D, Hassan C, et al. A prospective randomized study comparing 25-G and 22-G needles of a new platform for endoscopic ultrasound-guided fine needle aspiration of solid masses. Dig Liver Dis. 2016;48:49-54.

35. Guedes HG, Moura DTH, Duarte RB, Cordero MAC, Santos MELD, Cheng S, et al. A comparison of the efficiency of 22G versus 25G needles in EUS-FNA for solid pancreatic mass assessment: A systematic review and meta-analysis. Clinics. 2018;73:e261.
-3636. Park SW, Chung MJ, Lee SH, Lee HS, Lee HJ, Park JY, et al. Prospective Study for Comparison of Endoscopic Ultrasound-Guided Tissue Acquisition Using 25- and 22-Gauge Core Biopsy Needles in Solid Pancreatic Masses. PLoS One. 2016;11:e0154401.. Nevertheless, some recommendations agree on avoiding the 19-gauge needles in transduodenal punctures because it is less flexible and can be challenging to handle in this position3737. Laquière A, Lefort C, Maire F, Aubert A, Gincul R, Prat F, et al. 19 G nitinol needle versus 22 G needle for transduodenal endoscopic ultrasound-guided sampling of pancreatic solid masses: a randomized study. Endoscopy. 2019;51:436-43..

Novel devices for EUS-guided tissue sampling in pancreatic cystic lesions (PCL)

EUS-through-the-needle microforceps biopsy (EUS-TTNB) of the cystic wall in PCLs can differentiate between mucinous and non-mucinous neoplasms.

•Recommendation: B - 93.3% vote; evidence level 2a.

EUS-through-the-needle microforceps biopsy of PCLs is safe.

No agreement - 43.3% vote; evidence level 2c

Antibiotic prophylaxis in EUS-fine-needle aspiration of PCLs is not mandatory.

•Recommendation: B - 70% vote; evidence level 2a.

DISCUSSION

PCLs can be separated into pancreatic pseudocysts and epithelial cystic neoplasms, including mucinous and non-mucinous cysts. EUS is essential in differentiating between mucinous vs non-mucinous cysts and benign vs malignant lesions based on imaging features and EUS-FNA with biochemical analysis, cytopathological examination, and molecular biomarkers in the cystic liquid. However, this strategy has two significant limitations: Sometimes, it is impossible to aspirate enough liquid to perform these tests (especially in cysts smaller than 15 mm); these tests have low sensitivity for malignancy detection despite high specificity. Therefore, there is a growing interest in obtaining tissue sampling directly from the cyst wall with the emergence of multiple techniques for this purpose, notably EUS-TTNB.

Two systematic reviews (one with metanalysis) and two multicentric retrospective cohorts have demonstrated that EUS-TTNB of the cystic wall increased the diagnostic yield to differentiate between mucinous and non-mucinous pancreatic cystic lesions3838. Balaban VD, Cazacu IM, Pinte L, Jinga M, Bhutani MS, Saftoiu A. EUS-through-the-needle microbiopsy forceps in pancreatic cystic lesions: A systematic review. Endosc Ultrasound. 2021;10:19-24.

39. Barresi L, Crinò SF, Fabbri C, Attili F, Poley JW, Carrara S, et al. Endoscopic ultrasound-through-the-needle biopsy in pancreatic cystic lesions: A multicenter study. Dig Endosc. 2018;30:760-70.

40. Tacelli M, Celsa C, Magro B, Barchiesi M, Barresi L, Capurso G, et al. Diagnostic performance of endoscopic ultrasound through-the-needle microforceps biopsy of pancreatic cystic lesions: Systematic review with meta-analysis. Dig Endosc. 2020;32:1018-30.
-4141. Yang D, Samarasena JB, Jamil LH, Chang KJ, Lee D, Ona MA, et al. Endoscopic ultrasound-guided through-the-needle microforceps biopsy in the evaluation of pancreatic cystic lesions: a multicenter study. Endosc Int Open. 2018;6:E1423-E1430.. These studies showed that this procedure is feasible, has high technical success, and has better diagnostic performance than biochemical analysis of cystic needle aspiration. However, the adverse events rate ranges from 4% to 10% in the general population3838. Balaban VD, Cazacu IM, Pinte L, Jinga M, Bhutani MS, Saftoiu A. EUS-through-the-needle microbiopsy forceps in pancreatic cystic lesions: A systematic review. Endosc Ultrasound. 2021;10:19-24.,4040. Tacelli M, Celsa C, Magro B, Barchiesi M, Barresi L, Capurso G, et al. Diagnostic performance of endoscopic ultrasound through-the-needle microforceps biopsy of pancreatic cystic lesions: Systematic review with meta-analysis. Dig Endosc. 2020;32:1018-30.,4141. Yang D, Samarasena JB, Jamil LH, Chang KJ, Lee D, Ona MA, et al. Endoscopic ultrasound-guided through-the-needle microforceps biopsy in the evaluation of pancreatic cystic lesions: a multicenter study. Endosc Int Open. 2018;6:E1423-E1430., reaching up to 28% of pancreatitis in a subgroup including patients with more than 64 years, suspected IPMN, incomplete emptying of the cyst, and more than two passes through the needle4242. Facciorusso A, Kovacevic B, Yang D, Vilas-Boas F, Martínez-Moreno B, Stigliano S, et al. Predictors of adverse events after endoscopic ultrasound-guided through-the-needle biopsy of pancreatic cysts: a recursive partitioning analysis. Endoscopy. 2022;54:1158-68..

Many studies, including systematic reviews and meta-analyses, have recently been published on antibiotic prophylaxis in EUS-fine-needle aspiration of pancreatic cystic lesions. However, they did not prove its use decreases infectious complications in this setting4343. Hakim S, Gjeorgjievski M, Khan Z, Cannon ME, Yu K, Patil P, et al. Is antibiotic prophylaxis necessary after endoscopic ultrasound-guided fine-needle aspiration of pancreatic cysts? Clin Endosc. 2022;55:801-9.

44. Facciorusso A, Buccino VR, Turco A, Antonino M, Muscatiello N. Antibiotics Do Not Decrease the Rate of Infection After Endoscopic Ultrasound Fine-Needle Aspiration of Pancreatic Cysts. Dig Dis Sci. 2019;64:2308-15.

45. Colán-Hernández J, Sendino O, Loras C, Pardo A, Gornals JB, Concepción M, et al. Antibiotic Prophylaxis Is Not Required for Endoscopic Ultrasonography-Guided Fine-Needle Aspiration of Pancreatic Cystic Lesions, Based on a Randomized Trial. Gastroenterology. 2020;158:1642-1649.e1.
-4646. Palomera-Tejeda E, Shah H, Attar BM, Bhurwal A, Vohra I, Mutneja HR. Prophylactic Antibiotics Do Not Prevent Infectious Complications of Endoscopic Ultrasound Fine-Needle Aspiration of Pancreatic Cysts: A Systematic Review and Meta-Analysis. Pancreas. 2021;50:667-72..

EUS in the management of liver diseases and portal hypertension

EUS-guided liver biopsy still does not replace percutaneous liver biopsy.

•Recommendation: A - 90% vote; evidence level 1b.

EUS-guided portal pressure gradient (PPG) measurement is feasible and safe.

•Recommendation: C - 83.3% vote; evidence level 4.

EUS-guided therapy of gastric varices with coil and/or glue injection is feasible, safe, and superior to conventional endoscopic treatment.

•Recommendation: B - 90% vote; evidence level 2a.

DISCUSSION

With the development of EUS techniques and the increasing availability of them, an emerging field, endo hepatology, is gaining particular relevance. It focuses on diagnostic and therapeutic EUS applications in patients with liver diseases4747. Jearth V, Sundaram S, Rana SS. Diagnostic and interventional EUS in hepatology: An updated review. Endosc Ultrasound. 2022;11:355-70..

Although recent studies using core needles (EUS-FNB) demonstrate an improvement in histological sampling of EUS-guided liver biopsies, reducing the gap to the percutaneous liver biopsy, this latter method still provides more quality and amount of tissue (more significant number of complete portal tracts and specimens length)4848. Chandan S, Deliwala S, Khan SR, Mohan BP, Dhindsa BS, Bapaye J, et al. EUS-guided versus percutaneous liver biopsy: A comprehensive review and meta-analysis of outcomes. Endosc Ultrasound. 2023;12:171-80.

49. Ali AH, Nallapeta NS, Yousaf MN, Petroski GF, Sharma N, Rao DS, et al. EUS-guided versus percutaneous liver biopsy: A prospective randomized clinical trial. Endosc Ultrasound. 2023;12:334-41.

50. Rangwani S, Ardeshna DR, Mumtaz K, Kelly SG, Han SY, Krishna SG. Update on endoscopic ultrasound-guided liver biopsy. World J Gastroenterol. 2022;28:3586-94.
-5151. Johnson KD, Laoveeravat P, Yee EU, Perisetti A, Thandassery RB, Tharian B. Endoscopic ultrasound guided liver biopsy: Recent evidence. World J Gastrointest Endosc. 2020;12:83-97.. Additional advantages of EUS are that it allows a better study of the biliary tree anatomy and PPG measurement in the same procedure4747. Jearth V, Sundaram S, Rana SS. Diagnostic and interventional EUS in hepatology: An updated review. Endosc Ultrasound. 2022;11:355-70.. However, EUS-guided liver biopsies differ from the percutaneous method, and further studies with the new core tip needles are required.

EUS-guided PPG measurement is a procedure of growing interest in interventional EUS. In recent years, many studies have proved its feasibility and safety, with similar results to the transjugular technique and a low rate of adverse events4747. Jearth V, Sundaram S, Rana SS. Diagnostic and interventional EUS in hepatology: An updated review. Endosc Ultrasound. 2022;11:355-70.,5252. Samarasena JB, Yu AR, Chang KJ. EUS-guided portal pressure measurement (with videos). Endosc Ultrasound. 2018;7:257-62.,5353. Laleman W, Mertens J, Vanderschueren E, Praktiknjo M, Trebicka J. Advances in Endohepatology. Am J Gastroenterol. 2023;118:1756-67.. Considering these results and the increasing availability of techniques, EUS may shortly become the gold standard for evaluating PPG.

Concerning the treatment of gastric varices, since the last Consensus, new prospective studies and systematic reviews reinforced the efficacy and safety of EUS-guided therapy with injection of coil, cyanoacrylate, or both, showing lower adverse events and bleeding recurrence than the traditional method5454. Lôbo MRA, Chaves DM, DE Moura DTH, Ribeiro IB, Ikari E, DE Moura EGH. Safety and Efficacy of Eus-Guided Coil Plus Cyanoacrylate Versus Conventional Cyanoacrylate Technique In The Treatment Of Gastric Varices: A Randomized Controlled Trial. Arq Gastroenterol. 2019;56:99-105.

55. Mohan BP, Chandan S, Khan SR, Kassab LL, Trakroo S, Ponnada S, et al. Efficacy and safety of endoscopic ultrasound-guided therapy versus direct endoscopic glue injection therapy for gastric varices: systematic review and meta-analysis. Endoscopy. 2020;52:259-67.
-5656. McCarty TR, Bazarbashi AN, Hathorn KE, Thompson CC, Ryou M. Combination therapy versus monotherapy for EUS-guided management of gastric varices: A systematic review and meta-analysis. Endosc Ultrasound. 2020;9:6-15.. It is essential to note that most of these studies evaluated secondary prophylaxis even though other studies already demonstrated similar efficacy for primary prophylaxis5757. Kouanda A, Binmoeller K, Hamerski C, Nett A, Bernabe J, Shah J, et al. Safety and efficacy of EUS-guided coil and glue injection for the primary prophylaxis of gastric variceal hemorrhage. Gastrointest Endosc. 2021;94:291-6.. Some studies are still concerned with the efficacy of EUS-guided therapy for ectopic varices (duodenal, rectal) and thrombin injection5858. Frost JW, Hebbar S. EUS-guided thrombin injection for management of gastric fundal varices. Endosc Int Open. 2018;6:E664-E668., but all are in an initial phase, representing weak evidence.

EUS-biliary drainage

Bile duct drainage guided by ultrasound has technical success, clinical success, and adverse event rates similar to ERCP in patients with distal malignant biliary obstruction.

•Recommendation: A - 90% vote; evidence level 1a.

In cases of failed bile duct drainage by ERCP, both ultrasound-guided and percutaneous drainage show similar technical and clinical success rates but with fewer adverse events with the echooscopy-guided technique.

•Recommendation: A - 96.6% vote; evidence level 1a.

In cases of failed bile duct drainage by ERCP, when opting for ultrasound-guided access, both rendezvous and transparietal techniques show similar success rates and adverse events.

•Recommendation: B - 83.3% vote; evidence level 2b.

When opting for ultrasound-guided bile duct drainage using the rendezvous technique, access via the extrahepatic biliary route shows a higher success rate and fewer adverse events than intrahepatic access.

•Recommendation: B - 83.3% vote; evidence level 2b.

Ultrasound-guided transparietal bile duct drainage for distal malignant obstructions can be done via the choledocoduodenal or hepatogastric route. Both techniques show similar technical success rates, clinical success, and adverse events.

•Recommendation: B - 83.3% vote; evidence level 2b.

Ultrasound-guided bile duct drainage using the choledocoduodenal technique with either self-expanding metallic stent or appositional luminal stent shows similar technical success rates, clinical success, and adverse events.

•Recommendation: B - 86.6% vote; evidence level 2b.

DISCUSSION

Biliary drainage for distal malignant biliary obstructions via endoscopic retrograde cholangiopancreatography (ERCP) or guided by endoscopic ultrasound (EUS) shows similar rates of technical and clinical success5959. Kakked G, Salameh H, Cheesman AR, Kumta NA, Nagula S, DiMaio CJ. Primary EUS-guided biliary drainage versus ERCP drainage for the management of malignant biliary obstruction: A systematic review and meta-analysis. Endosc Ultrasound. 2020;9:298-307.

60. Lyu Y, Li T, Cheng Y, Wang B, Cao Y, Wang Y. Endoscopic ultrasound-guided vs ERCP-guided biliary drainage for malignant biliary obstruction: A up-to-date meta-analysis and systematic review. Dig Liver Dis. 2021;53:1247-53.

61. Li DF, Zhou CH, Wang LS, Yao J, Zou DW. Is ERCP-BD or EUS-BD the preferred decompression modality for malignant distal biliary obstruction? A meta-analysis of randomized controlled trials. Rev Esp Enferm Dig. 2019;111:953-60.

62. Park JK, Woo YS, Noh DH, Yang JI, Bae SY, Yun HS, Lee JK, et al. Efficacy of EUS-guided and ERCP-guided biliary drainage for malignant biliary obstruction: prospective randomized controlled study. Gastrointest Endosc. 2018;88:277-82.

63. Paik WH, Lee TH, Park DH, Choi JH, Kim SO, Jang S, et al. EUS-Guided Biliary Drainage Versus ERCP for the Primary Palliation of Malignant Biliary Obstruction: A Multicenter Randomized Clinical Trial. Am J Gastroenterol. 2018;113:987-97.
-6464. Teoh AYB, Napoleon B, Kunda R, Arcidiacono PG, Kongkam P, Larghi A, et al. EUS-Guided Choledocho-duodenostomy Using Lumen Apposing Stent Versus ERCP With Covered Metallic Stents in Patients With Unresectable Malignant Distal Biliary Obstruction: A Multicenter Randomized Controlled Trial (DRA-MBO Trial). Gastroenterology. 2023;165:473-482.e2.. However, some studies show higher rates of pancreatitis and reinterventions in the ERCP group5959. Kakked G, Salameh H, Cheesman AR, Kumta NA, Nagula S, DiMaio CJ. Primary EUS-guided biliary drainage versus ERCP drainage for the management of malignant biliary obstruction: A systematic review and meta-analysis. Endosc Ultrasound. 2020;9:298-307.

60. Lyu Y, Li T, Cheng Y, Wang B, Cao Y, Wang Y. Endoscopic ultrasound-guided vs ERCP-guided biliary drainage for malignant biliary obstruction: A up-to-date meta-analysis and systematic review. Dig Liver Dis. 2021;53:1247-53.

61. Li DF, Zhou CH, Wang LS, Yao J, Zou DW. Is ERCP-BD or EUS-BD the preferred decompression modality for malignant distal biliary obstruction? A meta-analysis of randomized controlled trials. Rev Esp Enferm Dig. 2019;111:953-60.

62. Park JK, Woo YS, Noh DH, Yang JI, Bae SY, Yun HS, Lee JK, et al. Efficacy of EUS-guided and ERCP-guided biliary drainage for malignant biliary obstruction: prospective randomized controlled study. Gastrointest Endosc. 2018;88:277-82.

63. Paik WH, Lee TH, Park DH, Choi JH, Kim SO, Jang S, et al. EUS-Guided Biliary Drainage Versus ERCP for the Primary Palliation of Malignant Biliary Obstruction: A Multicenter Randomized Clinical Trial. Am J Gastroenterol. 2018;113:987-97.
-6464. Teoh AYB, Napoleon B, Kunda R, Arcidiacono PG, Kongkam P, Larghi A, et al. EUS-Guided Choledocho-duodenostomy Using Lumen Apposing Stent Versus ERCP With Covered Metallic Stents in Patients With Unresectable Malignant Distal Biliary Obstruction: A Multicenter Randomized Controlled Trial (DRA-MBO Trial). Gastroenterology. 2023;165:473-482.e2.. Nonetheless, only some randomized studies compare the two techniques, which prevents us from stating that EUS-guided biliary drainage can be considered the procedure of choice for distal malignant biliary obstruction. In failed ERCP biliary drainage cases, two EUS-guided drainage techniques are available: transluminal and rendezvous. Few studies comparing the two techniques show similar success and adverse event rates6565. Khashab MA, Valeshabad AK, Modayil R, Widmer J, Saxena P, Idrees M, et al. EUS-guided biliary drainage by using a standardized approach for malignant biliary obstruction: rendezvous versus direct transluminal techniques (with videos). Gastrointest Endosc. 2013;78:734-41..

Both EUS-guided and percutaneous biliary drainage show similar technical and clinical success rates in cases of failed ERCP drainage6666. Sharaiha RZ, Khan MA, Kamal F, Tyberg A, Tombazzi CR, Ali B, et al. Efficacy and safety of EUS-guided biliary drainage in comparison with percutaneous biliary drainage when ERCP fails: a systematic review and meta-analysis. Gastrointest Endosc. 2017;85:904-14.

67. Hayat U, Bakker C, Dirweesh A, Khan MY, Adler DG, Okut H, et al. EUS-guided versus percutaneous transhepatic cholangiography biliary drainage for obstructed distal malignant biliary strictures in patients who have failed endoscopic retrograde cholangiopancreatography: A systematic review and meta-analysis. Endosc Ultrasound. 2022;11:4-16.

68. Hassan Z, Gadour E. Percutaneous transhepatic cholangiography vs endoscopic ultrasound-guided biliary drainage: A systematic review. World J Gastroenterol. 2022;28:3514-23.

69. Sawas T, Bailey NJ, Yeung KYKA, James TW, Reddy S, Fleming CJ, et al. Comparison of EUS-guided choledochoduodenostomy and percutaneous drainage for distal biliary obstruction: A multicenter cohort study. Endosc Ultrasound. 2022;11:223-30.

70. Khashab MA, Valeshabad AK, Afghani E, Singh VK, Kumbhari V, Messallam A, et al. A comparative evaluation of EUS-guided biliary drainage and percutaneous drainage in patients with distal malignant biliary obstruction and failed ERCP. Dig Dis Sci. 2015;60:557-65.

71. Artifon EL, Aparicio D, Paione JB, Lo SK, Bordini A, Rabello C, et al. Biliary drainage in patients with unresectable, malignant obstruction where ERCP fails: endoscopic ultrasonography-guided choledochoduodenostomy versus percutaneous drainage. J Clin Gastroenterol. 2012;46:768-74.
-7272. Sportes A, Camus M, Greget M, Leblanc S, Coriat R, Hochberger J, et al. Endoscopic ultrasound-guided hepaticogastrostomy versus percutaneous transhepatic drainage for malignant biliary obstruction after failed endoscopic retrograde cholangiopancreatography: a retrospective expertise-based study from two centers. Therap Adv Gastroenterol. 2017;10:483-93.. However, EUS-guided drainage generally has lower rates of adverse events and re-interventions6666. Sharaiha RZ, Khan MA, Kamal F, Tyberg A, Tombazzi CR, Ali B, et al. Efficacy and safety of EUS-guided biliary drainage in comparison with percutaneous biliary drainage when ERCP fails: a systematic review and meta-analysis. Gastrointest Endosc. 2017;85:904-14.

67. Hayat U, Bakker C, Dirweesh A, Khan MY, Adler DG, Okut H, et al. EUS-guided versus percutaneous transhepatic cholangiography biliary drainage for obstructed distal malignant biliary strictures in patients who have failed endoscopic retrograde cholangiopancreatography: A systematic review and meta-analysis. Endosc Ultrasound. 2022;11:4-16.

68. Hassan Z, Gadour E. Percutaneous transhepatic cholangiography vs endoscopic ultrasound-guided biliary drainage: A systematic review. World J Gastroenterol. 2022;28:3514-23.

69. Sawas T, Bailey NJ, Yeung KYKA, James TW, Reddy S, Fleming CJ, et al. Comparison of EUS-guided choledochoduodenostomy and percutaneous drainage for distal biliary obstruction: A multicenter cohort study. Endosc Ultrasound. 2022;11:223-30.

70. Khashab MA, Valeshabad AK, Afghani E, Singh VK, Kumbhari V, Messallam A, et al. A comparative evaluation of EUS-guided biliary drainage and percutaneous drainage in patients with distal malignant biliary obstruction and failed ERCP. Dig Dis Sci. 2015;60:557-65.

71. Artifon EL, Aparicio D, Paione JB, Lo SK, Bordini A, Rabello C, et al. Biliary drainage in patients with unresectable, malignant obstruction where ERCP fails: endoscopic ultrasonography-guided choledochoduodenostomy versus percutaneous drainage. J Clin Gastroenterol. 2012;46:768-74.
-7272. Sportes A, Camus M, Greget M, Leblanc S, Coriat R, Hochberger J, et al. Endoscopic ultrasound-guided hepaticogastrostomy versus percutaneous transhepatic drainage for malignant biliary obstruction after failed endoscopic retrograde cholangiopancreatography: a retrospective expertise-based study from two centers. Therap Adv Gastroenterol. 2017;10:483-93.. The choice of technique should be made after multidisciplinary discussion and according to local availability and experience. When both techniques are available, preference should be given to EUS-guided drainage.

Few studies compare access via the extrahepatic biliary tract with access via the intrahepatic route for rendezvous drainage, most with small sample sizes7373. Iwashita T, Lee JG, Shinoura S, Nakai Y, Park DH, Muthusamy VR, et al. Endoscopic ultrasound-guided rendezvous for biliary access after failed cannulation. Endoscopy. 2012;44:60-5.

74. Dhir V, Bhandari S, Bapat M, Joshi N, Vivekanandarajah S, Maydeo A. Comparison of transhepatic and extrahepatic routes for EUS-guided rendezvous procedure for distal CBD obstruction. United European Gastroenterol J. 2013;1:103-8.

75. Dhir V, Artifon EL, Gupta K, Vila JJ, Maselli R, Frazao M, et al. Multicenter study on endoscopic ultrasound-guided expandable biliary metal stent placement: choice of access route, direction of stent insertion, and drainage route. Dig Endosc. 2014;26:430-5.
-7676. Park DH, Jeong SU, Lee BU, Lee SS, Seo DW, Lee SK, et al. Prospective evaluation of a treatment algorithm with enhanced guidewire manipulation protocol for EUS-guided biliary drainage after failed ERCP (with video). Gastrointest Endosc. 2013;78:91-101.. A trend toward higher success rates and fewer adverse events with extrahepatic access is indicated. However, better-quality studies are needed to reach a definitive conclusion.

EUS-guided biliary drainage via the choledocoduodenal and hepatogastric routes shows similar technical and clinical success rates for distal biliary obstructions. Regarding adverse events, both techniques have similar rates in most studies, although some show fewer adverse events and reinterventions for obstruction with the choledocoduodenal technique7777. Li J, Tang J, Liu F, Fang J. Comparison of Choledochoduodenostomy and Hepaticogastrostomy for EUS-Guided Biliary Drainage: A Meta-Analysis. Front Surg. 2022;9:811005.

78. Mao K, Hu B, Sun F, Wan K. Choledochoduodenostomy Versus Hepaticogastrostomy in Endoscopic Ultrasound-guided Drainage for Malignant Biliary Obstruction: A Meta-analysis and Systematic Review. Surg Laparosc Endosc Percutan Tech. 2021;32:124-32.

79. Minaga K, Ogura T, Shiomi H, Imai H, Hoki N, Takenaka M, et al. Comparison of the efficacy and safety of endoscopic ultrasound-guided choledochoduodenostomy and hepaticogastrostomy for malignant distal biliary obstruction: Multicenter, randomized, clinical trial. Dig Endosc. 2019;31:575-82.

80. Yamazaki H, Yamashita Y, Shimokawa T, Minaga K, Ogura T, Kitano M. Endoscopic ultrasound-guided hepaticogastrostomy versus choledochoduodenostomy for malignant biliary obstruction: A meta-analysis. DEN Open. 2023;4:e274.
-8181. Artifon EL, Marson FP, Gaidhane M, Kahaleh M, Otoch JP. Hepaticogastrostomy or choledochoduodenostomy for distal malignant biliary obstruction after failed ERCP: is there any difference? Gastrointest Endosc. 2015;81:950-9.. However, more prospective and randomized studies comparing the two approaches are needed. It is important to note that the hepatogastric route can be used for biliary drainage in both high and low obstructions, while the choledocoduodenal technique is restricted to distal obstructions.

Plastic stents, previously used for choledocoduodenal drainage, have been abandoned in favor of metal stents due to many adverse events, mainly biliary fistula and stent dysfunction8282. de Benito Sanz M, Nájera-Muñoz R, de la Serna-Higuera C, Fuentes-Valenzuela E, Fanjul I, Chavarría C, et al. Lumen apposing metal stents versus tubular self-expandable metal stents for endoscopic ultrasound-guided choledochoduodenostomy in malignant biliary obstruction. Surg Endosc. 2021;35:6754-62.. Currently, two models of metal stents can be used in this technique: the fully or partially covered self-expanding stent and the lumen-apposing stent. Few studies comparing the two models suggest similar technical and clinical success rates and adverse events8383. Amato A, Sinagra E, Celsa C, Enea M, Buda A, Vieceli F, et al. Efficacy of lumen-apposing metal stents or self-expandable metal stents for endoscopic ultrasound-guided choledochoduodenostomy: a systematic review and meta-analysis. Endoscopy. 2021;53:1037-47..

EUS-guided management of pancreatic fluid collection

Endoscopic ultrasound can differentially diagnose neoplastic pancreatic cysts and detect necrosis before indicating drainage.

•Recommendation: B - 96.6% vote; evidence level 2c.

Ultrasound-guided drainage of pancreatic pseudocysts: Plastic and metallic stents have similar outcomes.

•Recommendation: B - 86.6% vote; evidence level 2c.

Using metallic stents with luminal apposition is not the first choice for draining pancreatic pseudocysts.

•Recommendation: B - 73.3% vote; evidence level 2c.

LAMS are preferable to plastic stents for draining Walled-off Necrosis (WON).

•Recommendation: B - 100% vote; evidence level 2a.

A correlation exists between the LAMS remaining in place for more than 4 weeks and a higher incidence of adverse events.

•Recommendation: B - 80% vote; evidence level 2c.

Plastic pigtail-type stents inside the LAMS for draining Walled-off Necrosis (WON) reduce the risk of adverse events.

•Recommendation: B - 53.3% vote; evidence level 3b.

DISCUSSION

Endoscopic ultrasound (EUS) plays a crucial role in the differential diagnosis of pancreatic cystic lesions and detecting intracystic necrosis8484. Siddiqui AA, Kowalski TE, Loren DE, Khalid A, Soomro A, Mazhar SM, et al. Fully covered self-expanding metal stents versus lumen-apposing fully covered self-expanding metal stent versus plastic stents for endoscopic drainage of pancreatic walled-off necrosis: clinical outcomes and success. Gastrointest Endosc. 2017;85:758-65.

85. Itoi T, Binmoeller KF, Shah J, Sofuni A, Itokawa F, Kurihara T, et al. Clinical evaluation of a novel lumen-apposing metal stent for endosonography-guided pancreatic pseudocyst and gallbladder drainage (with videos). Gastrointest Endosc. 2012;75:870-6.
-8686. Rinninella E, Kunda R, Dollhopf M, Sanchez-Yague A, Will U, Tarantino I, et al. EUS-guided drainage of pancreatic fluid collections using a novel lumen-apposing metal stent on an electrocautery-enhanced delivery system: a large retrospective study (with video). Gastrointest Endosc. 2015;82:1039-46.. The rates of resolution, adverse events, and recurrences are similar (85%, 20%, and 10%, respectively) among the different stents used for pseudocyst drainage8484. Siddiqui AA, Kowalski TE, Loren DE, Khalid A, Soomro A, Mazhar SM, et al. Fully covered self-expanding metal stents versus lumen-apposing fully covered self-expanding metal stent versus plastic stents for endoscopic drainage of pancreatic walled-off necrosis: clinical outcomes and success. Gastrointest Endosc. 2017;85:758-65.

85. Itoi T, Binmoeller KF, Shah J, Sofuni A, Itokawa F, Kurihara T, et al. Clinical evaluation of a novel lumen-apposing metal stent for endosonography-guided pancreatic pseudocyst and gallbladder drainage (with videos). Gastrointest Endosc. 2012;75:870-6.

86. Rinninella E, Kunda R, Dollhopf M, Sanchez-Yague A, Will U, Tarantino I, et al. EUS-guided drainage of pancreatic fluid collections using a novel lumen-apposing metal stent on an electrocautery-enhanced delivery system: a large retrospective study (with video). Gastrointest Endosc. 2015;82:1039-46.

87. Lee BU, Song TJ, Lee SS, Park DH, Seo DW, Lee SK, et al. Newly designed, fully covered metal stents for endoscopic ultrasound (EUS)-guided transmural drainage of peripancreatic fluid collections: a prospective randomized study. Endoscopy. 2014;46:1078-84.
-8888. Bhasin DK, Rana SS, Nanda M, Chandail VS, Gupta R, Kang M, et al. Comparative evaluation of transpapillary drainage with nasopancreatic drain and stent in patients with large pseudocysts located near tail of pancreas. J Gastrointest Surg. 2011;15:772-6.. The results of lumen-apposing metal stents (LAMS) in pancreatic pseudocyst drainage are promising but have not yet demonstrated superiority over other stents8484. Siddiqui AA, Kowalski TE, Loren DE, Khalid A, Soomro A, Mazhar SM, et al. Fully covered self-expanding metal stents versus lumen-apposing fully covered self-expanding metal stent versus plastic stents for endoscopic drainage of pancreatic walled-off necrosis: clinical outcomes and success. Gastrointest Endosc. 2017;85:758-65.

85. Itoi T, Binmoeller KF, Shah J, Sofuni A, Itokawa F, Kurihara T, et al. Clinical evaluation of a novel lumen-apposing metal stent for endosonography-guided pancreatic pseudocyst and gallbladder drainage (with videos). Gastrointest Endosc. 2012;75:870-6.

86. Rinninella E, Kunda R, Dollhopf M, Sanchez-Yague A, Will U, Tarantino I, et al. EUS-guided drainage of pancreatic fluid collections using a novel lumen-apposing metal stent on an electrocautery-enhanced delivery system: a large retrospective study (with video). Gastrointest Endosc. 2015;82:1039-46.

87. Lee BU, Song TJ, Lee SS, Park DH, Seo DW, Lee SK, et al. Newly designed, fully covered metal stents for endoscopic ultrasound (EUS)-guided transmural drainage of peripancreatic fluid collections: a prospective randomized study. Endoscopy. 2014;46:1078-84.
-8888. Bhasin DK, Rana SS, Nanda M, Chandail VS, Gupta R, Kang M, et al. Comparative evaluation of transpapillary drainage with nasopancreatic drain and stent in patients with large pseudocysts located near tail of pancreas. J Gastrointest Surg. 2011;15:772-6..

Despite LAMS are gradually replacing plastic stents, there is currently no high-quality evidence to recommend LAMS use for WON drainage exclusively. The most recent meta-analyses on the topic demonstrated similar clinical success rates (LAMS 88.5% vs plastic 88.1%) and similar adverse events (LAMS 11.2% vs plastic 15.9%) between both types of stents8989. Bazerbachi F, Sawas T, Vargas EJ, Prokop LJ, Chari ST, Gleeson FC, et al. Metal stents versus plastic stents for the management of pancreatic walled-off necrosis: a systematic review and meta-analysis. Gastrointest Endosc. 2018;87:30-42.e15.. Although more studies are needed for better definition, LAMS are preferably chosen because they allow easy access to the walled-off necrosis (WON) cavity for inspection and necrosectomy without the need for stent removal/exchange, as well as shorter procedure time and fewer interventions required for WON resolution9090. Chandrasekhara V, Barthet M, Devière J, Bazerbachi F, Lakhtakia S, Easler JJ, et al. Safety and efficacy of lumen-apposing metal stents versus plastic stents to treat walled-off pancreatic necrosis: systematic review and meta-analysis. Endosc Int Open. 2020;8:E1639-E1653.

91. Chen YI, Yang J, Friedland S, Holmes I, Law R, Hosmer A, et al. Lumen apposing metal stents are superior to plastic stents in pancreatic walled-off necrosis: a large international multicenter study. Endosc Int Open. 2019;7:E347-E354.
-9292. Fugazza A, Sethi A, Trindade AJ, Troncone E, Devlin J, Khashab MA, et al. International multicenter comprehensive analysis of adverse events associated with lumen-apposing metal stent placement for pancreatic fluid collection drainage. Gastrointest Endosc. 2020;91:574-83..

The risk of adverse events related to LAMS always needs consideration before drainage, and an extended stent dwell time would be associated with higher risks. Despite that, a retrospective analysis of a larger multicenter database recently published showed that longer stent dwell time (4-8 weeks vs >8 weeks) did not increase the risk of late adverse events, such as bleeding and stent burial syndrome, providing indirect evidence for maintaining LAMS in situ beyond 4 weeks9292. Fugazza A, Sethi A, Trindade AJ, Troncone E, Devlin J, Khashab MA, et al. International multicenter comprehensive analysis of adverse events associated with lumen-apposing metal stent placement for pancreatic fluid collection drainage. Gastrointest Endosc. 2020;91:574-83.. Besides that, despite the theoretical benefit of reducing adverse events with the combination of double-pigtail stents and LAMS for WON management, recent studies have not shown a significant difference in occlusion and migration rates of LAMS, infection and bleeding9191. Chen YI, Yang J, Friedland S, Holmes I, Law R, Hosmer A, et al. Lumen apposing metal stents are superior to plastic stents in pancreatic walled-off necrosis: a large international multicenter study. Endosc Int Open. 2019;7:E347-E354..

EUS-gastroenterostomy

EUS-GE is the preferred treatment over duodenal stent for malignant gastric outlet obstruction in centers with expertise, especially in patients with a life expectancy higher than 2 months.

•Recommendation: B - 90% vote; evidence level 2b.

In selected patients (life expectancy >2 months, without voluminous ascites), EUS-GE can be preferable over surgical gastrojejunostomy to treat malignant gastric outlet obstruction.

•Recommendation: B - 100% vote; evidence level 2b.

There is still no gold standard technique for performing EUS-GE.

•Recommendation: B - 93.3% vote; evidence level 3b.

The 20 mm lumen-apposing metal stent (LAMS) is the best size for EUS-GE.

•Recommendation: B - 83.3% vote; evidence level 3a.

DISCUSSION

Echo-guided gastrojejunostomy (EUS-GE) demonstrates a technical success rate similar to duodenal stenting. However, it shows better clinical outcomes (98% vs 91%) and a lower rate of adverse events (8.6% vs 38.9%)9393. Jaruvongvanich V, Mahmoud T, Abu Dayyeh BK, Chandrasekhara V, Law R, Storm AC, et al. Endoscopic ultrasound-guided gastroenterostomy for the management of gastric outlet obstruction: A large comparative study with long-term follow-up. Endosc Int Open. 2023;11:E60-E66.. Another advantage of EUS-GE over duodenal stenting is the recurrence rate of obstruction. At 6 months, obstruction recurrence in the EUS-GE group was 1.7% compared to 28% in the duodenal stenting group9494. Teoh AYB, Lakhtakia S, Tarantino I, Perez-Miranda M, Kunda R, Maluf-Filho F, et al. Endoscopic ultrasonography-guided gastroenterostomy versus uncovered duodenal metal stenting for unresectable malignant gastric outlet obstruction (DRA-GOO): a multicentre randomised controlled trial. Lancet Gastroenterol Hepatol. 2024;9:124-32.. Also, EUS-guided gastrojejunostomy (EUS-GE) demonstrates technical and clinical success rates similar to surgical gastrojejunostomy. Besides that, it offers advantages such as a shorter time to oral intake initiation, shorter hospitalization duration, lower adverse event rates, and shorter time to resume chemotherapy. One disadvantage is the higher reintervention rate (15% vs 1.6%), requiring expertise and a standardized technique9595. Krishnamoorthi R, Bomman S, Benias P, Kozarek RA, Peetermans JA, McMullen E, et al. Efficacy and safety of endoscopic duodenal stent versus endoscopic or surgical gastrojejunostomy to treat malignant gastric outlet obstruction: systematic review and meta-analysis. Endosc Int Open. 2022;10:E874-E897.,9696. Canakis A, Bomman S, Lee DU, Ross A, Larsen M, Krishnamoorthi R, et al. Benefits of EUS-guided gastroenterostomy over surgical gastrojejunostomy in the palliation of malignant gastric outlet obstruction: a large multicenter experience. Gastrointest Endosc. 2023;98:348-359.e30..

Technical options for performing echo-guided gastrojejunostomy include the wire-guided technique (with or without balloon assistance) and the balloon-assisted technique. Although few studies compare the available techniques for echo-guided gastrojejunostomy, the wire-guided technique shows lower technical success rates associated with a higher complication rate9797. Monino L, Perez-Cuadrado-Robles E, Gonzalez JM, Snauwaert C, Alric H, Gasmi M, et al. Endoscopic ultrasound-guided gastroenterostomy with lumen-apposing metal stents: a retrospective multicentric comparison of wireless and over-the-wire techniques. Endoscopy. 2023;55:991-9.. There is no study comparing balloon-assisted versus balloon-free techniques, requiring further research for technique standardization.

Both available LAMS (lumen-apposing metal stents) diameters (15 mm and 20 mm) are safe and effective for clinically successful gastrojejunostomy, with similar technical success rates and adverse effects. The 20 mm LAMS diameter is similar to the physiological gastric outlet (20 to 23 mm) and the surgical gastrojejunostomy diameter. Consequently, it has a lower reintervention rate than the 15 mm LAMS, making it the recommended stent9898. Vedantam S, Shah R, Bhalla S, Kumar S, Amin S. No difference in outcomes with 15 mm vs. 20 mm lumen-apposing metal stents for endoscopic ultrasound-guided gastroenterostomy for gastric outlet obstruction: a meta-analysis. Clin Endosc. 2023;56:298-307.. Patients with a 20 mm stent tolerated a more consistent diet9999. Bejjani M, Ghandour B, Subtil JC, Martínez-Moreno B, Sharaiha RZ, Watson RR, et al. Clinical and technical outcomes of patients undergoing endoscopic ultrasound-guided gastroenterostomy using 20-mm vs. 15-mm lumen-apposing metal stents. Endoscopy. 2022;54:680-7..

EUS-guided radiofrequecy ablation of pancreatic neoplasms

There is a clinical response and low adverse events with EUS-RFA for treating pancreatic tumors.

•Recommendation: B - 83.3% vote; evidence level 3a.

RFA treatment for NETs shows promising results in both functioning and non-functioning types, with a higher tendency for success in functioning NETs (especially insulinoma).

•Recommendation: B - 100% vote; evidence level 2a.

Both techniques are effective and safe compared to ethanol ablation and RFA in NETs, which have similar outcomes.

•Recommendation: B - 66.6% vote; evidence level 2a.

There are doubts and a lack of evidence regarding using EUS-RFA to improve survival in pancreatic adenocarcinoma.

•Recommendation: B - 100% vote; evidence level 3a.

There is not enough evidence demonstrating the benefit of treating pancreatic cystic lesions with radiofrequency ablation.

•Recommendation: B - 96.6% vote; evidence level 3a.

DISCUSSION

The use of RFA for pancreatic tumors is associated with a high clinical response and low rates of adverse events100100. Fahmawi Y, Mehta A, Abdalhadi H, Merritt L, Mizrahi M. Efficacy and safety of endoscopic ultrasound-guided radiofrequency ablation for management of pancreatic lesions: a systematic review and meta-analysis. Transl Gastroenterol Hepatol. 2022;7:30.. In a recent meta-analysis comparing EUS-RFA treatment for functional (F-NET) and non-functional (NF-NET) neuroendocrine tumors, high efficacy rates were shown (95.1% vs 93.4%, respectively). The procedures had low rates of moderate or severe adverse events but notable rates of mild events, reaching approximately 20%101101. Armellini E, Facciorusso A, Crinò SF. Efficacy and Safety of Endoscopic Ultrasound-Guided Radiofrequency Ablation for Pancreatic Neuroendocrine Tumors: A Systematic Review and Metanalysis. Medicina (Kaunas). 2023;59:359.. Besides that, when comparing the treatment of NETs with RFA and ethanol, similar results were presented in a systematic review and meta-analysis102102. Imperatore N, de Nucci G, Mandelli ED, de Leone A, Zito FP, Lombardi G, et al. Endoscopic ultrasound-guided radiofrequency ablation of pancreatic neuroendocrine tumors: a systematic review of the literature. Endosc Int Open. 2020;8:E1759-E1764..

A prospective Chinese study evaluated 22 patients with unresectable pancreatic adenocarcinoma treated with EUS-RFA103103. Oh D, Seo DW, Song TJ, Park DH, Lee SK, Kim MH. Clinical outcomes of EUS-guided radiofrequency ablation for unresectable pancreatic cancer: A prospective observational study. Endosc Ultrasound. 2022;11:68-74.. There were no severe adverse events, and 3.74% experienced mild to moderate events such as abdominal pain and peritonitis. They also demonstrated statistically significant overall and progression-free survival, 24.03 months and 16.37 months, respectively (level of evidence 3b). However, robust studies are lacking to support this hypothesis.

When comparing techniques for ablation of pancreatic cystic lesions (PCLs), the meta-analysis published in the journal Cancers by Pereira et al. showed relatively unpromising data regarding EUS-RFA compared to other techniques, such as ethanol utilization, with only a 13% success rate104104. Papaefthymiou A, Johnson GJ, Maida M, Gkolfakis P, Ramai D, Facciorusso A, et al. Performance and Safety of EUS Ablation Techniques for Pancreatic Cystic Lesions: A Systematic Review and Meta-Analysis. Cancers (Basel). 2023;15:2627..

CONCLUSION

There is moderate evidence to support that the needle shape, gauge, or aspiration technique does not influence the yield of EUS-guided tissue sampling of pancreatic solid lesions. There is moderate evidence to support the use of microforceps biopsy of the cyst wall to differentiate between mucous and serous cystic neoplasms. There is a low level of evidence to support the routine use of EUS-guided treatment of gastric varices. There is a high level of evidence to support that EUS-guided biliary drainage and ERCP present similar clinical success and adverse event rates in patients with distal malignant biliary obstruction. There is evidence for using EUS to differentially diagnose neoplastic pancreatic cysts and detect necrosis before indicating drainage. There is moderate evidence to support EUS-GE over duodenal stent for malignant gastric outlet obstruction in patients with a life expectancy higher than 2 months. There is a high level of evidence to support the use of RFA in treating both functioning and non-functioning types of NET.

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  • Disclosure of funding:

    none
  • Declaration of use of artificial intelligence:

    none

Edited by

Associate Editor:

Ricardo Guilherme Viebig.

Publication Dates

  • Publication in this collection
    21 Oct 2024
  • Date of issue
    2024

History

  • Received
    04 Aug 2024
  • Accepted
    20 Aug 2024
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