A Novel Endoscopic Ultrasonography Imaging Technique for Depicting Microcirculation in Pancreatobiliary Lesions without the Need for Contrast-Enhancement: A Prospective Exploratory Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Patients
2.2. Study Design
2.3. EUS Procedure
2.4. DFI-EUS
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ahmad, N.A.; Kochman, M.L.; Lewis, J.D.; Kadish, S.; Morris, J.B.; Rosato, E.F.; Ginsberg, G.G. Endosonography is superior to angiography in the preoperative assessment of vascular involvement among patients with pancreatic carcinoma. J. Clin. Gastroenterol. 2001, 32, 54–58. [Google Scholar] [CrossRef]
- DeWitt, J.; Devereaux, B.; Chriswell, M.; McGreevy, K.; Howard, T.; Imperiale, T.F.; Ciaccia, D.; Lane, K.A.; Maglinte, D.; Kopecky, K.; et al. Comparison of endoscopic ultrasonography and multidetector computed tomography for detecting and staging pancreatic cancer. Ann. Intern. Med. 2004, 141, 753–763. [Google Scholar] [CrossRef] [Green Version]
- Zuccaro, G.; Sterling, M.J. Endosonography in pancreatic disease: Differential diagnosis. In Gastrointest Endoscopy; Van Dam, J., Sivak, M.V., Eds.; Saunders: Philadelphia, PA, USA, 1999; pp. 235–243. [Google Scholar]
- Das, K.; Kudo, M.; Kitano, M.; Sakamoto, H.; Komaki, T.; Takagi, T.; Yamao, K. Diagnostic value of endoscopic ultrasound-guided directional eFLOW in solid pancreatic lesions. J. Med. Ultrason. 2013, 40, 211–218. [Google Scholar] [CrossRef]
- Yamashita, Y.; Kato, J.; Ueda, K.; Nakamura, Y.; Kawaji, Y.; Abe, H.; Nuta, J.; Tamura, T.; Itonaga, M.; Yoshida, T.; et al. Contrast-Enhanced Endoscopic Ultrasonography for Pancreatic Tumors. Biomed Res. Int. 2015, 491782. [Google Scholar] [CrossRef]
- Kitano, M.; Kudo, M.; Yamao, K.; Takagi, T.; Sakamoto, H.; Komaki, T.; Kamata, K.; Imai, H.; Chiba, Y.; Okada, M.; et al. Characterization of small solid tumors in the pancreas: The value of contrast-enhanced harmonic endoscopic ultrasonography. Am. J. Gastroenterol. 2012, 107, 303–310. [Google Scholar] [CrossRef]
- Omoto, S.; Takenaka, M.; Kitano, M.; Miyata, T.; Kamata, K.; Minaga, K.; Arizumi, T.; Yamao, K.; Imai, H.; Sakamoto, H.; et al. Characterization of Pancreatic Tumors with Quantitative Perfusion Analysis in Contrast-Enhanced Harmonic Endoscopic Ultrasonography. Oncology 2017, 93 (Suppl. S1), 55–60. [Google Scholar] [CrossRef]
- Yamashita, Y.; Tanioka, K.; Kawaji, Y.; Tamura, T.; Nuta, J.; Hatamaru, K.; Itonaga, M.; Yoshida, T.; Ida, Y.; Maekita, T.; et al. Utility of Contrast-Enhanced Harmonic Endoscopic Ultrasonography for Early Diagnosis of Small Pancreatic Cancer. Diagnostics 2020, 10, 23. [Google Scholar] [CrossRef] [Green Version]
- Omoto, S.; Kitano, M.; Fukasawa, M.; Ashida, R.; Kato, H.; Shiomi, H.; Sugimori, K.; Kanno, A.; Chiba, Y.; Takano, S.; et al. Tissue Harmonic versus Contrast-Enhanced Harmonic Endoscopic Ultrasonography for the diagnosis of Pancreatic Tumors: A Prospective Multicenter Study. Dig. Endosc 2021. Early View. [Google Scholar] [CrossRef]
- Yamashita, Y.; Shimokawa, T.; Napoléon, B.; Fusaroli, P.; Gincul, R.; Kudo, M.; Kitano, M. Value of contrast-enhanced harmonic endoscopic ultrasonography with enhancement pattern for diagnosis of pancreatic cancer: A meta-analysis. Dig. Endosc. 2019, 31, 125–133. [Google Scholar] [CrossRef]
- Yamamoto, N.; Kato, H.; Tomoda, T.; Matsumoto, K.; Sakakihara, I.; Noma, Y.; Horiguchi, S.; Harada, R.; Tsutsumi, K.; Hori, K.; et al. Contrast-enhanced harmonic endoscopic ultrasonography with time-intensity curve analysis for intraductal papillary mucinous neoplasms of the pancreas. Endoscopy 2016, 48, 26–34. [Google Scholar] [CrossRef] [Green Version]
- Kamata, K.; Kitano, M.; Omoto, S.; Kadosaka, K.; Miyata, T.; Yamao, K.; Imai, H.; Sakamoto, H.; Harwani, Y.; Chikugo, T.; et al. Contrast-enhanced harmonic endoscopic ultrasonography for differential diagnosis of pancreatic cysts. Endoscopy 2016, 48, 35–41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamashita, Y.; Ueda, K.; Itonaga, M.; Yoshida, T.; Maeda, H.; Maekita, T.; Iguchi, M.; Tamai, H.; Ichinose, M.; Kato, J. Usefulness of contrast-enhanced endoscopic sonography for discriminating mural nodules from mucous clots in intraductal papillary mucinous neoplasms: A single-center prospective study. J. Ultrasound. Med. 2013, 32, 61–68. [Google Scholar] [CrossRef] [PubMed]
- Fujita, M.; Itoi, T.; Ikeuchi, N.; Sofuni, A.; Tsuchiya, T.; Ishii, K.; Kamada, K.; Umeda, J.; Tanaka, R.; Tonozuka, R.; et al. Effectiveness of contrast-enhanced endoscopic ultrasound for detecting mural nodules in intraductal papillary mucinous neoplasm of the pancreas and for making therapeutic decisions. Endosc. Ultrasound. 2016, 5, 377–383. [Google Scholar]
- Harima, H.; Kaino, S.; Shinoda, S.; Kawano, M.; Suenaga, S.; Sakaida, I. Differential diagnosis of benign and malignant branch duct intraductal papillary mucinous neoplasm using contrast-enhanced endoscopic ultrasonography. World J. Gastroenterol. 2015, 21, 6252–6260. [Google Scholar] [CrossRef]
- Kamata, K.; Takenaka, M.; Kitano, M.; Omoto, S.; Miyata, T.; Minaga, K.; Yamao, K.; Imai, H.; Sakurai, T.; Nishida, N.; et al. Contrast-enhanced harmonic endoscopic ultrasonography for differential diagnosis of localized gallbladder lesions. Dig. Endosc. 2018, 30, 98–106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Imazu, H.; Mori, N.; Kanazawa, K.; Chiba, M.; Toyoizumi, H.; Torisu, Y.; Koyama, S.; Hino, S.; Ang, T.L.; Tajiri, H. Contrast-enhanced harmonic endoscopic ultrasonography in the differential diagnosis of gallbladder wall thickening. Dig. Dis. Sci. 2014, 59, 1909–1916. [Google Scholar] [CrossRef]
- Liang, X.; Jing, X. Meta-analysis of contrast-enhanced ultrasound and contrast-enhanced harmonic endoscopic ultrasound for the diagnosis of gallbladder malignancy. BMC Med. Inform. Decis. Mak. 2020, 20, 235. [Google Scholar] [CrossRef]
- Fusaroli, P.; Spada, A.; Mancino, M.G.; Caletti, G. Contrast harmonic echo-endoscopic ultrasound improves accuracy in diagnosis of solid pancreatic masses. Clin. Gastroenterol. Hepatol. 2010, 8, 629–634. [Google Scholar] [CrossRef] [PubMed]
- Hocke, M.; Ignee, A.; Dietrich, C.F. Advanced endosonographic diagnostic tools for discrimination of focal chronic pancreatitis and pancreatic carcinoma—elastography, contrast enhanced high mechanical index (CEHMI) and low mechanical index (CELMI) endosonography in direct comparison. Z Gastroenterol. 2012, 50, 199–203. [Google Scholar] [CrossRef] [PubMed]
- Yamashita, Y.; Kitano, M.; Ashida, R. Value of endoscopy for early diagnosis of pancreatic carcinoma. Dig. Endosc. 2020, 32, 27–36. [Google Scholar] [CrossRef] [Green Version]
- Kitano, M.; Yoshida, T.; Itnonaga, M.; Tamura, T.; Hatamaru, K.; Yamashita, Y. Impact of endoscopic ultrasonography on diagnosis of pancreatic cancer. J. Gastroenterol. 2019, 54, 19–32. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, T.; Yamashita, Y.; Kitano, M. Endoscopic Ultrasound for Early Diagnosis of Pancreatic Cancer. Diagnostics 2019, 9, 81. [Google Scholar] [CrossRef] [Green Version]
- Scientific Discussion; European Medicines Agency: Amsterdam, The Netherlands, 2004; CPMP/0053/01.
- Yamashita, Y.; Yoshikawa, T.; Kawaji, Y.; Tamura, T.; Hatamaru, K.; Itonaga, M.; Ida, Y.; Maekita, T.; Iguchi, M.; Murata, S.I.; et al. Novel endoscopic ultrasonography imaging technique for visualizing microcirculation without contrast enhancement in subepithelial lesions: Prospective study. Dig. Endosc. 2020, 33. [Google Scholar] [CrossRef]
- Jensen, J.A. Estimation of Blood Velocities Using Ultrasound: A Signal Processing Approach; Cambridge University Press: New York, NY, USA, 1996. [Google Scholar]
- Lu, R.; Meng, Y.; Zhang, Y.; Zhao, W.; Wang, X.; Jin, M.; Guo, R. Superb microvascular imaging (SMI) compared with conventional ultrasound for evaluating thyroid nodules. BMC Med. Imaging 2017, 28, 65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bakdik, S.; Arslan, S.; Oncu, F.; Durmaz, M.S.; Altunkeser, A.; Eryilmaz, M.A.; Unlu, Y. Effectiveness of Superb Microvascular Imaging for the differentiation of intraductal breast lesions. Med. Ultrason. 2018, 20, 306–312. [Google Scholar] [CrossRef] [Green Version]
- Dubinsky, T.J.; Revels, J.; Wang, S.; Toia, G.; Sonneborn, R.; Hippe, D.S.; Erpelding, T. Comparison of Superb Microvascular Imaging with Color Flow and Power Doppler Imaging of Small Hepatocellular Carcinomas. J. Ultrasound. Med. 2018, 37, 2915–2924. [Google Scholar] [CrossRef]
- Mao, Y.; Mu, J.; Zhao, J.; Zhao, L.; Xin, X. The value of superb microvascular imaging in differentiating benign renal mass from malignant renal tumor: A retrospective study. Br. J. Radiol. 2018, 91, 20170601. [Google Scholar] [CrossRef] [PubMed]
- Sim, J.K.; Lee, J.Y.; Hong, H.S. Differentiation Between Malignant and Benign Lymph Nodes: Role of Superb Microvascular Imaging in the Evaluation of Cervical Lymph Nodes. J. Ultrasound. Med. 2019, 38, 3025–3036. [Google Scholar] [CrossRef] [PubMed]
- Kuroda, H.; Abe, T.; Kakisaka, K.; Fujiwara, Y.; Yoshida, Y.; Miyasaka, A.; Ishida, K.; Ishida, H.; Sugai, T.; Takikawa, Y. Visualizing the hepatic vascular architecture using superb microvascular imaging in patients with hepatitis C virus: A novel technique. World J. Gastroenterol. 2016, 22, 6057–6064. [Google Scholar] [CrossRef] [PubMed]
Characteristic | |
---|---|
Median age (range), years | 69 (20–90) |
Sex (male:female) | 23/30 |
Diagnosis | |
Pancreatic cancer | 23 |
Inflammatory mass | 8 |
Solid papillary neoplasm | 2 |
Neuroendocrine tumor | 1 |
Intraductal papillary mucinous neoplasm | 8 |
Gallbladder cancer | 2 |
Cholesterol polyp | 3 |
Chronic cholecystitis | 1 |
Gallbladder sludge | 3 |
Benign lymph node | 4 |
DFI-EUS | e-FLOW EUS | CE-EUS | |
---|---|---|---|
Pancreatic cancer | 83% (19/23) | 52% (12/23) | 100% (23/23) |
Neuroendocrine tumor | 100% (1/1) | 100% (1/1) | 100% (1/1) |
Solid papillary neoplasm | 100% (2/2) | 50% (1/2) | 100% (2/2) |
IPMN with mural nodule | 100% (2/2) | 0% (0/2) | 100% (2/2) |
IPMC | 100% (1/1) | 0% (0/1) | 100% (1/1) |
IPMN with mucous clot | 0% (0/5) | 0% (0/5) | 0% (0/5) |
Inflammatory mass | 100% (8/8) | 63% (5/8) | 100% (8/8) |
Malignant lymph node | 100% (1/1) | 100% (1/1) | 100% (1/1) |
Benign lymph node | 100% (3/3) | 67% (2/3) | 100% (3/3) |
Gallbladder cancer | 100% (2/2) | 50% (1/2) | 100% (2/2) |
Gallbladder cholesterol polyp | 100% (1/1) | 0% (0/1) | 100% (1/1) |
Chronic cholecystitis | 100% (1/1) | 100% (1/1) | 100% (1/1) |
Gallbladder sludge | 0% (0/3) | 0% (0/3) | 0% (0/3) |
Vessels Positive on CE-EUS | Vessels Negative on CE-EUS | |
---|---|---|
Vessels positive on DFI-EUS | 41 | 0 |
Vessels negative on DFI-EUS | 4 | 8 |
Vessels Positive on CE-EUS | Vessels Negative on CE-EUS | |
---|---|---|
Vessels positive on e-FLOW EUS | 24 | 0 |
Vessels negative on e-FLOW EUS | 21 | 8 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yamashita, Y.; Yoshikawa, T.; Yamazaki, H.; Kawaji, Y.; Tamura, T.; Hatamaru, K.; Itonaga, M.; Ashida, R.; Ida, Y.; Maekita, T.; et al. A Novel Endoscopic Ultrasonography Imaging Technique for Depicting Microcirculation in Pancreatobiliary Lesions without the Need for Contrast-Enhancement: A Prospective Exploratory Study. Diagnostics 2021, 11, 2018. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112018
Yamashita Y, Yoshikawa T, Yamazaki H, Kawaji Y, Tamura T, Hatamaru K, Itonaga M, Ashida R, Ida Y, Maekita T, et al. A Novel Endoscopic Ultrasonography Imaging Technique for Depicting Microcirculation in Pancreatobiliary Lesions without the Need for Contrast-Enhancement: A Prospective Exploratory Study. Diagnostics. 2021; 11(11):2018. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112018
Chicago/Turabian StyleYamashita, Yasunobu, Takanori Yoshikawa, Hirofumi Yamazaki, Yuki Kawaji, Takashi Tamura, Keiichi Hatamaru, Masahiro Itonaga, Reiko Ashida, Yoshiyuki Ida, Takao Maekita, and et al. 2021. "A Novel Endoscopic Ultrasonography Imaging Technique for Depicting Microcirculation in Pancreatobiliary Lesions without the Need for Contrast-Enhancement: A Prospective Exploratory Study" Diagnostics 11, no. 11: 2018. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112018