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CC BY-NC-ND 4.0 · Endosc Int Open 2024; 12(03): E361-E366
DOI: 10.1055/a-2257-3171
Original article

Comparison of endoscopic ultrasound-guided fine-needle aspiration and fine-needle biopsy to generate pancreatic cancer organoids: Randomized trial

Johannes Roman Wiessner 
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Felix Orben
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Arlett Schäfer
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Lisa Fricke
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Günter Schneider
2   Department of General, Visceral and Pediatric Surgery, University Medical Center Göttingen, Gottingen, Germany (Ringgold ID: RIN27177)
3   Klinikum rechts der Isar, School of Medicine, Technical University of Munich, Chair of Translational Cancer Research and Institute of Experimental Cancer Therapy, München, Germany
4   CCC-N (Comprehensive Cancer Center Lower Saxony), Medizinische Hochschule Hannover, Hannover, Germany (Ringgold ID: RIN9177)
,
Maximilian Reichert
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
5   Translational Pancreatic Cancer Center, Medical Clinic and Polyclinic II, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
6   German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Partner Site Munich, DKFZ, Heidelberg, Germany (Ringgold ID: RIN28333)
7   Center for Protein Assemblies (CPA), Technical University of Munich, 85747, Garching, Germany (Ringgold ID: RIN9184)
,
Alexander Herner
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
8   Department of Gastroenterology and Hepatology, University Hospital Zurich, Zürich, Switzerland (Ringgold ID: RIN27243)
,
Ulrich Mayr
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Veit Phillip
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Matthias Treiber
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Guido von Figura
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Mohamed Abdelhafez
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Roland M. Schmid
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
,
Christoph Schlag
8   Department of Gastroenterology and Hepatology, University Hospital Zurich, Zürich, Switzerland (Ringgold ID: RIN27243)
1   Medical Clinic and Polyclinic II, Klinikum rechts der Isar, Technical University of Munich, München, Germany (Ringgold ID: RIN9184)
› Author AffiliationsSupported by: Deutsche Forschungsgemeinschaft SFB1321 (Project-ID 329628492), RE 3723/4-1
Supported by: Deutsche Krebshilfe Max-Eder Program 111273 and 70114328

Clinical Trial: Registration number (trial ID): NCT03990675, Trial registry: ClinicalTrials.gov (http://www.clinicaltrials.gov/), Type of Study: Prospective randomized
› Further Information
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Abstract

Background and study aims The prognosis for pancreatic cancer remains poor. Molecular diagnostics and customized therapies are becoming increasingly important in clinical routine. Patient-derived, predictive model systems such as organoids have the potential to substantially increase the depth of information from biopsy material by functional and molecular characterization. We compared the extent to which the use of fine-needle aspiration needles (FNA, 22G) or fine-needle biopsy needles (FNB, 22G) influences the generation of pancreatic cancer patient-derived organoids (PDOs) to establish endoscopic standards of organoid technology.

Patients and methods Endoscopic ultrasound (EUS)-guided punctures by EUS-FNA and EUS-FNB of pancreatic masses highly suspicious for adenocarcinoma (detected by computed tomography and/or magnetic resonance imaging) were prospectively evaluated. Consecutive patients received EUS-FNA and EUS-FNB in a randomized order without the need to exchange the needle shaft (only the inner needle type (FNA/-B) was exchanged) between the passes. With each needle type, the specimens for histological analysis and for PDOs were obtained separately.

Results Fifty patients were enrolled in the study. Histology revealed malignancy in 42 of 50 cases (84%). In total PDOs were generated from 17 patients (34%). Of these, nine were established by FNB only, two by FNA only, and six by both FNA and FNB. Histology revealed malignancy in 13 of 17 PDO cases (76%). In two histologically false-negative cases, PDOs could be established.

Conclusions EUS-FNB was superior to EUS-FNA in terms of successful generation of PDOs, although it failed to show statistical significance.

Keywords

Endoscopic ultrasonography - Pancreas - Tissue diagnosis - Fine-needle aspiration/biopsy


Publication History

Received: 18 July 2023

Accepted after revision: 19 December 2023

Article published online:
07 March 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

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  • References

  • 1 Roser M, Ritchie H. Cancer. Our World Data. https://ourworldindata.org/cancer
    PubMed
  • 2 Hidalgo M. Pancreatic cancer. N Engl J Med 2010; 362: 1605-1617
    CrossrefPubMedSearch in Google Scholar
  • 3 Strobel O, Neoptolemos J, Jäger D. et al. Optimizing the outcomes of pancreatic cancer surgery. Nat Rev Clin Oncol 2019; 16: 11-26
    CrossrefPubMedSearch in Google Scholar
  • 4 Khorana AA, Mangu PB, Berlin J. et al. Potentially curable pancreatic cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 2016; 34: 2541-2556
    CrossrefPubMedSearch in Google Scholar
  • 5 Ma J, Jemal A. The rise and fall of cancer mortality in the USA: why does pancreatic cancer not follow the trend?. Future Oncol 2013; 9: 917-919
    CrossrefPubMedSearch in Google Scholar
  • 6 Schmidt KT, Chau CH, Price DK. et al. Precision oncology medicine: The clinical relevance of patient-specific biomarkers used to optimize cancer treatment. J Clin Pharmacol 2016; 56: 1484-1499
    CrossrefPubMedSearch in Google Scholar
  • 7 Moreira L, Bakir B, Chatterji P. et al. Pancreas 3D organoids: Current and future aspects as a research platform for personalized medicine in pancreatic cancer. Cell Mol Gastroenterol Hepatol 2018; 5: 289-298
    CrossrefPubMedSearch in Google Scholar
  • 8 Dantes Z, Yen HY, Pfarr N. et al. Implementing cell-free DNA of pancreatic cancer patient-derived organoids for personalized oncology. JCI Insight 2020; 5
    CrossrefPubMedSearch in Google Scholar
  • 9 Huang L, Holtzinger A, Jagan I. et al. Ductal pancreatic cancer modeling and drug screening using human pluripotent stem cell- and patient-derived tumor organoids. Nat Med 2015; 21: 1364-1371
    CrossrefPubMedSearch in Google Scholar
  • 10 Peschke K, Jakubowsky H, Schäfer A. et al. Identification of treatment-induced vulnerabilities in pancreatic cancer patients using functional model systems. EMBO Mol Med 2022; 14: e14876
    CrossrefPubMedSearch in Google Scholar
  • 11 Tiriac H, Bucobo JC, Tzimas D. et al. Successful creation of pancreatic cancer organoids by means of EUS-guided fine-needle biopsy sampling for personalized cancer treatment. Gastrointest Endosc 2018; 87: 1474-1480
    CrossrefPubMedSearch in Google Scholar
  • 12 Kandel P, Tranesh G, Nassar A. et al. EUS-guided fine needle biopsy sampling using a novel fork-tip needle: a case-control study. Gastrointest Endosc 2016; 84: 1034-1039
    CrossrefPubMedSearch in Google Scholar
  • 13 DiMaio CJ, Kolb JM, Benias PC. et al. Initial experience with a novel EUS-guided core biopsy needle (SharkCore): results of a large North American multicenter study. Endosc Int Open 2016; 4: E974-979
    Thieme ConnectPubMedSearch in Google Scholar
  • 14 Oppong KW, Bekkali NLH, Leeds JS. et al. Fork-tip needle biopsy versus fine-needle aspiration in endoscopic ultrasound-guided sampling of solid pancreatic masses: a randomized crossover study. Endoscopy 2020; 52: 454-461
    Thieme ConnectPubMedSearch in Google Scholar
  • 15 Karsenti D, Palazzo L, Perrot B. et al. 22G Acquire vs. 20G Procore needle for endoscopic ultrasound-guided biopsy of pancreatic masses: a randomized study comparing histologic sample quantity and diagnostic accuracy. Endoscopy 2020; 52: 747-753
    Thieme ConnectPubMedSearch in Google Scholar
  • 16 Tian L, Tang AL, Zhang L. 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: 3533-3539
    CrossrefPubMedSearch in Google Scholar
  • 17 Jones S, Zhang X, Parsons DW. et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321: 1801-1806
    CrossrefPubMedSearch in Google Scholar
  • 18 Wei S, Lieberman D, Morrissette JJD. et al. Using ‘residual’ FNA rinse and body fluid specimens for next-generation sequencing: An institutional experience. Cancer Cytopathol 2016; 124: 324-329
    CrossrefPubMedSearch in Google Scholar
  • 19 Boj SF, Hwang CI, Baker LA. et al. Organoid models of human and mouse ductal pancreatic cancer. Cell 2015; 160: 324-338
    CrossrefPubMedSearch in Google Scholar
  • 20 Juiz N, Elkaoutari A, Bigonnet M. et al. Basal-like and classical cells coexist in pancreatic cancer revealed by single-cell analysis on biopsy-derived pancreatic cancer organoids from the classical subtype. FASEB J Off Publ Fed Am Soc Exp Biol 2020; 34: 12214-12228
    PubMedSearch in Google Scholar
  • 21 Asokkumar R, Yung Ka C, Loh T. 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 22 Ishida Y, Tsunoda T, Hamada Y. et al. Standardized methods using EUS-guided fine-needle biopsy and a minimal medium creates three pancreatic cancer organoids. Anticancer Res 2022; 42: 4103-4109
    CrossrefPubMedSearch in Google Scholar
  • 23 Lacomb JF, Plenker D, Tiriac H. et al. Single-pass vs 2-pass endoscopic ultrasound-guided fine-needle biopsy sample collection for creation of pancreatic adenocarcinoma organoids. Clin Gastroenterol Hepatol 2021; 19: 845-847
    CrossrefPubMedSearch in Google Scholar