The Use of Endoscopic Ultrasonography in Inflammatory Bowel Disease: A Review of the Literature
Abstract
1. Introduction
2. Materials and Methods
3. Perianal Crohn’s Disease
4. Differentiating Ulcerative Colitis and Crohn’s Disease
5. Monitoring the Activity of Inflammatory Bowel Disease
6. EUS and Inflammatory-Bowel-Disease-Related Complications
7. Limitations of EUS in Inflammatory Bowel Disease
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Lew, R.J.; Ginsberg, G.G. The role of endoscopic ultrasound in inflammatory bowel disease. Gastrointest. Endosc. Clin. N. Am. 2002, 12, 561–571. [Google Scholar] [CrossRef] [PubMed]
- Tremaine, W.J. Is indeterminate colitis determinable? Curr. Gastroenterol. Rep. 2012, 14, 162–165. [Google Scholar] [CrossRef] [PubMed]
- Flynn, S.; Eisenstein, S. Inflammatory Bowel Disease Presentation and Diagnosis. Surg. Clin. North Am. 2019, 99, 1051–1062. [Google Scholar] [CrossRef] [PubMed]
- Bo, S. Atlas of Endoscopy Imaging in Inflammatory Bowel Disease; Academic Press: Cambridge, MA, USA, 2020; pp. 129–146. [Google Scholar]
- Kucharzik, T.; Tielbeek, J.; Carter, D.; Taylor, S.; Tolan, D.; Wilkens, R.; Bryant, R.V.; Hoeffel, C.; De Kock, I.; Maaser, C.; et al. ECCO-ESGAR Topical Review on Optimizing Reporting for Cross-Sectional Imaging in Inflammatory Bowel Disease. J. Crohns. Colitis. 2022, 16, 523–543. [Google Scholar] [CrossRef]
- Dambha, F.; Tanner, J.; Carroll, N. Diagnostic imaging in Crohn’s disease: What is the new gold standard? Best Pract. Res. Clin. Gastroenterol. 2014, 28, 421–436. [Google Scholar] [CrossRef]
- Hasak, S.; Kushnir, V. Rectal Endoscopic Ultrasound in Clinical Practice. Curr. Gastroenterol. Rep. 2019, 12, 18. [Google Scholar] [CrossRef]
- Okasha, H.H.; Pawlak, K.M.; Abou-Elmagd, A.; El-Meligui, A.; Atalla, H.; Othman, M.O.; Elenin, S.A.; Alzamzamy, A.; Mahdy, R.E. Practical approach to linear endoscopic ultrasound examination of the rectum and anal canal. Endosc. Int. Open. 2022, 10, E1417–E1426. [Google Scholar] [CrossRef]
- Menzel, J.; Domschke, W. Gastrointestinal miniprobe sonography: The current status. Am. J. Gastroenterol. 2000, 95, 605–616. [Google Scholar] [CrossRef]
- Tsuga, K.; Haruma, K.; Fujimura, J.; Hata, J.; Tani, H.; Tanaka, S.; Sumii, K.; Kajiyama, G. Evaluation of the colorectal wall in normal subjects and patients with ulcerative colitis using an ultrasonic catheter probe. Gastrointest. Endosc. 1998, 48, 477–484. [Google Scholar] [CrossRef]
- Steinhart, A.H.; Panaccione, R.; Targownik, L.; Bressler, B.; Khanna, R.; Marshall, J.K.; Afif, W.; Bernstein, C.N.; Bitton, A.; Borgaonkar, M.; et al. Clinical Practice Guideline for the Medical Management of Perianal Fistulizing Crohn’s Disease: The Toronto Consensus. J. Can. Assoc. Gastroenterol. 2018, 1, 141–154. [Google Scholar] [CrossRef]
- Gajendran, M.; Loganathan, P.; Catinella, A.P.; Hashash, J.G. A comprehensive review and update on Crohn’s disease. Dis. Mon. 2018, 64, 20–57. [Google Scholar] [CrossRef] [PubMed]
- Safar, B.; Sands, D. Perianal Crohn’s disease. Clin. Colon. Rectal. Surg. 2007, 20, 282–293. [Google Scholar] [CrossRef] [PubMed]
- Molteni, R.D.A.; Bonin, E.A.; Baldin Júnior, A.; Barreto, R.A.Y.; Brenner, A.S.; Lopes, T.L.; Volpato, A.P.D.J.; Sartor, M.C. Usefulness of endoscopic ultrasound for perianal fistula in Crohn’s disease. Papel da ultrassonografia endoscópica na avaliação da fístula perianal na doença de Crohn. Rev. Col. Bras Cir. 2019, 45, e1840. [Google Scholar] [CrossRef] [PubMed]
- Lamb, C.A.; Kennedy, N.A.; Raine, T.; Hendy, P.A.; Smith, P.J.; Limdi, J.K.; Hayee, B.; Lomer, M.C.E.; Parkes, G.C.; Selinger, C.; et al. British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 2019, 68 (Suppl. 3), s1–s106, Erratum in Gut 2021, 70, 1. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, D.A.; Wiersema, M.J.; Dudiak, K.M.; Fletcher, J.G.; Clain, J.E.; Tremaine, W.J.; Zinsmeister, A.R.; Norton, I.D.; Boardman, L.A.; Devine, R.M.; et al. A comparison of endoscopic ultrasound, magnetic resonance imaging, and exam under anesthesia for evaluation of Crohn’s perianal fistulas. Gastroenterology 2001, 121, 1064–1072. [Google Scholar] [CrossRef] [PubMed]
- Makowiec, F.; Laniado, M.; Jehle, E.C.; Claussen, C.D.; Starlinger, M. Magnetic resonance imaging in perianal Crohn’s disease. Inflamm. Bowel Dis. 1995, 1, 256–265. [Google Scholar] [CrossRef]
- Orsoni, P.; Barthet, M.; Portier, F.; Panuel, M.; Desjeux, A.; Grimaud, J.C. Prospective comparison of endosonography, magnetic resonance imaging and surgical findings in anorectal fistula and abscess complicating Crohn’s disease. Br. J. Surg. 1999, 86, 360–364. [Google Scholar] [CrossRef]
- Siddiqui, M.R.S.; Ashrafian, H.; Tozer, P.; Daulatzai, N.; Burling, D.; Hart, A.; Athanasiou, T.; Phillips, R.K. A diagnostic accuracy meta-analysis of endoanal ultrasound and MRI for perianal fistula assessment. Dis. Colon. Rectum. 2012, 55, 576–585. [Google Scholar] [CrossRef]
- Wise, P.E.; Schwartz, D.A. The evaluation and treatment of Crohn perianal fistulae: EUA, EUS, MRI, and other imaging modalities. Gastroenterol. Clin. North Am. 2012, 41, 379–391. [Google Scholar] [CrossRef]
- Poen, A.C.; Felt-Bersma, R.J.; Eijsbouts, Q.A.; Cuesta, M.A.; Meuwissen, S.G. Hydrogen peroxide-enhanced transanal ultrasound in the assessment of fistula-in-ano. Dis. Colon. Rectum. 1998, 41, 1147–1152. [Google Scholar] [CrossRef]
- Sloots, C.E.; Felt-Bersma, R.J.; Poen, A.C.; Cuesta, M.A.; Meuwissen, S.G. Assessment and classification of fistula-in-ano in patients with Crohn’s disease by hydrogen peroxide enhanced transanal ultrasound. Int. J. Colorectal. Dis. 2001, 16, 292–297. [Google Scholar] [CrossRef]
- Navarro-Luna, A.; García-Domingo, M.I.; Rius-Macías, J.; Marco-Molina, C. Ultrasound study of anal fistulas with hydrogen peroxide enhancement. Dis. Colon. Rectum. 2004, 47, 108–114. [Google Scholar] [CrossRef] [PubMed]
- Tsankov, T.; Tankova, L.; Deredjan, H.; Kovatchki, D. Contrast-enhanced endoanal and transperineal sonography in perianal fistulas. Hepatogastroenterology 2008, 55, 13–16. [Google Scholar] [PubMed]
- Zawadzki, A.; Starck, M.; Bohe, M.; Thorlacius, H. A unique 3D endoanal ultrasound feature of perianal Crohn’s fistula: The ‘Crohn ultrasound fistula sign’. Colorectal Dis. 2012, 14, e608–e611. [Google Scholar] [CrossRef] [PubMed]
- Luglio, G.; Giglio, M.C.; Rispo, A.; Bucci, C.; Sollazzo, V.; Castiglione, F.; De Palma, G.D.; Bucci, L. Diagnostic Accuracy of 3-Dimensional Endoanal Ultrasound in Identifying Perianal Crohn’s Fistulas. Dis. Colon. Rectum. 2018, 61, 931–937. [Google Scholar] [CrossRef]
- West, R.L.; Dwarkasing, S.; Felt-Bersma, R.J.; Schouten, W.R.; Hop, W.C.; Hussain, S.M.; Kuipers, E.J. Hydrogen peroxide-enhanced three-dimensional endoanal ultrasonography and endoanal magnetic resonance imaging in evaluating perianal fistulas: Agreement and patient preference. Eur. J. Gastroenterol. Hepatol. 2004, 16, 1319–1324. [Google Scholar] [CrossRef]
- Chew, S.S.; Yang, J.L.; Newstead, G.L.; Douglas, P.R. Anal fistula: Levovist-enhanced endoanal ultrasound: A pilot study. Dis. Colon. Rectum. 2003, 46, 377–384. [Google Scholar] [CrossRef]
- Ardizzone, S.; Maconi, G.; Cassinotti, A.; Massari, A.; Porro, G.B. Imaging of perianal Crohn’s disease. Dig. Liver Dis. 2007, 39, 970–978. [Google Scholar] [CrossRef]
- Schwartz, D.A.; White, C.M.; Wise, P.E.; Herline, A.J. Use of endoscopic ultrasound to guide combination medical and surgical therapy for patients with Crohn’s perianal fistulas. Inflamm. Bowel Dis. 2005, 11, 727–732. [Google Scholar] [CrossRef]
- Guidi, L.; Ratto, C.; Semeraro, S.; Roberto, I.; De Vitis, I.; Papa, A.; Marzo, M.; Parello, A.; Foglietto, G.; Doglietto, G.B.; et al. Combined therapy with infliximab and seton drainage for perianal fistulizing Crohn’s disease with anal endosonographic monitoring: A single-centre experience. Tech. Coloproctol. 2008, 12, 111–117. [Google Scholar] [CrossRef]
- Ardizzone, S.; Maconi, G.; Colombo, E.; Manzionna, G.; Bollani, S.; Bianchi Porro, G. Perianal fistulae following infliximab treatment: Clinical and endosonographic outcome. Inflamm. Bowel Dis. 2004, 10, 91–96. [Google Scholar] [CrossRef] [PubMed]
- Spradlin, N.M.; Wise, P.E.; Herline, A.J.; Muldoon, R.L.; Rosen, M.; Schwartz, D.A. A randomized prospective trial of endoscopic ultrasound to guide combination medical and surgical treatment for Crohn’s perianal fistulas. Am. J. Gastroenterol. 2008, 103, 2527–2535. [Google Scholar] [CrossRef] [PubMed]
- Limberg, B. Diagnosis of acute ulcerative colitis and colonic Crohn’s disease by colonic sonography. J. Clin. Ultrasound. 1989, 17, 25–31. [Google Scholar] [CrossRef] [PubMed]
- Hildebrandt, U.; Kraus, J.; Ecker, K.W.; Schmid, T.; Schüder, G.; Feifel, G. Endosonographic differentiation of mucosal and transmural nonspecific inflammatory bowel disease. Endoscopy 1992, 24 (Suppl. 1), 359–363. [Google Scholar] [CrossRef] [PubMed]
- Gast, P.; Belaïche, J. Rectal endosonography in inflammatory bowel disease: Differential diagnosis and prediction of remission. Endoscopy 1999, 31, 158–166. [Google Scholar] [CrossRef]
- Ellrichmann, M.; Wietzke-Braun, P.; Dhar, S.; Nikolaus, S.; Arlt, A.; Bethge, J.; Kuehbacher, T.; Wintermeyer, L.; Balschun, K.; Klapper, W.; et al. Endoscopic ultrasound of the colon for the differentiation of Crohn’s disease and ulcerative colitis in comparison with healthy controls. Aliment. Pharmacol. Ther. 2014, 39, 823–833. [Google Scholar] [CrossRef]
- Roushan, N.; Daryani, N.E.; Azizi, Z.; Pournaghshband, H.; Niksirat, A. Differentiation of Crohn’s disease and ulcerative colitis using intestinal wall thickness of the colon: A Diagnostic accuracy study of endoscopic ultrasonography. Med. J. Islam. Repub. Iran. 2019, 33, 57. [Google Scholar] [CrossRef]
- Rustemovic, N.; Cukovic-Cavka, S.; Brinar, M.; Radić, D.; Opacic, M.; Ostojic, R.; Vucelic, B. A pilot study of transrectal endoscopic ultrasound elastography in inflammatory bowel disease. BMC Gastroenterol. 2011, 11, 113. [Google Scholar] [CrossRef]
- Rasmussen, S.N.; Riis, P. Rectal wall thickness measured by ultrasound in chronic inflammatory diseases of the colon. Scand. J. Gastroenterol. 1985, 20, 109–114. [Google Scholar] [CrossRef]
- Dağli, U.; Over, H.; Tezel, A.; Ulker, A.; Temuçin, G. Transrectal ultrasound in the diagnosis and management of inflammatory bowel disease. Endoscopy 1999, 31, 152–157. [Google Scholar] [CrossRef]
- Soweid, A.M.; Chak, A.; Katz, J.A.; Sivak, M.V., Jr. Catheter probe assisted endoluminal US in inflammatory bowel disease. Gastrointest. Endosc. 1999, 50, 41–46. [Google Scholar] [CrossRef] [PubMed]
- Rana, S.S.; Kante, B.; Shah, J.; Nada, R.; Kalra, N.; Gupta, R. Role of EUS in idiopathic ulcerative colitis. Endosc. Ultrasound. 2021, 10, 313–314. [Google Scholar] [CrossRef] [PubMed]
- Cho, E.; Mochizuki, N.; Ashihara, T.; Yasuda, K.; Nakajima, M. Endoscopic ultrasonography in the evaluation of inflammatory bowel disease. Endoscopy 1998, 30 (Suppl. 1), A94–A96. [Google Scholar] [CrossRef] [PubMed]
- Cho, E.; Yasuda, K.; Nakajima, M. EUS in the diagnosis of ulcerative colitis. Dig. Endosc. 2004, 16, S182–S184. [Google Scholar] [CrossRef]
- Matts, S.G. The value of rectal biopsy in the diagnosis of ulcerative colitis. Q. J. Med. 1961, 30, 393–407. [Google Scholar]
- Hurlstone, D.P.; Sanders, D.S.; Lobo, A.J.; McAlindon, M.E.; Cross, S.S. Prospective evaluation of high-frequency mini-probe ultrasound colonoscopic imaging in ulcerative colitis: A valid tool for predicting clinical severity. Eur. J. Gastroenterol. Hepatol. 2005, 17, 1325–1331. [Google Scholar] [CrossRef]
- Yan, B.; Feagan, B.; Teriaky, A.; Mosli, M.; Mohamed, R.; Williams, G.; Yeung, E.; Yong, E.; Haig, A.; Sey, M.; et al. Reliability of EUS indices to detect inflammation in ulcerative colitis. Gastrointest. Endosc. 2017, 86, 1079–1087. [Google Scholar] [CrossRef]
- Jin, R.F.; Chen, Y.M.; Chen, R.P.; Ye, H.J. Endoscopic ultrasonography in the evaluation of condition and prognosis of ulcerative colitis. World J. Clin. Cases. 2022, 10, 4818–4826. [Google Scholar] [CrossRef]
- Higaki, S.; Nohara, H.; Saitoh, Y.; Akazawa, A.; Yanai, H.; Yoshida, T.; Okita, K. Increased rectal wall thickness may predict relapse in ulcerative colitis: A pilot follow-up study by ultrasonographic colonoscopy. Endoscopy 2002, 34, 212–219. [Google Scholar] [CrossRef]
- Watanabe, O.; Ando, T.; El-Omar, E.; Shimada, M.; Ina, K.; Ishiguro, K.; Hasegawa, M.; Miyake, N.; Nakamura, M.; Miyahara, R.; et al. Role of endoscopic ultrasonography in predicting the response to cyclosporin A in ulcerative colitis refractory to steroids. Dig. Liver Dis. 2009, 41, 735–739. [Google Scholar] [CrossRef]
- Yoshizawa, S.; Kobayashi, K.; Katsumata, T.; Saigenji, K.; Okayasu, I. Clinical usefulness of EUS for active ulcerative colitis. Gastrointest. Endosc. 2007, 65, 253–260. [Google Scholar] [CrossRef]
- Shimizu, S.; Myojo, S.; Nagashima, M.; Okuyama, Y.; Sugeta, N.; Sakamoto, S.; Kutsumi, H.; Otsuka, H.; Suyama, Y.; Fujimoto, S. A patient with rectal cancer associated with ulcerative colitis in whom endoscopic ultrasonography was useful for diagnosis. J. Gastroenterol. 1999, 34, 516–519. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, K.; Kawagishi, K.; Ooka, S.; Yokoyama, K.; Sada, M.; Koizumi, W. Clinical usefulness of endoscopic ultrasonography for the evaluation of ulcerative colitis-associated tumors. World J. Gastroenterol. 2015, 21, 2693–2699. [Google Scholar] [CrossRef] [PubMed]
- Mohy-Ud-Din, N.; Kochhar, G.; Dhawan, M. Endoscopic Ultrasound Guided Drainage of a Post-Surgical Fluid Collection Using a Lumen-Apposing Metal Stent in a Patient with Crohn’s Disease. ACG Case Rep. J. 2020, 7, e00290. [Google Scholar] [CrossRef]
- Teoh, A.Y.; Lee, J.F.; Chong, C.C.; Tang, R.S. Endoscopic ultrasonography-guided drainage of a rectal mucocele after total colectomy for Crohn’s disease. Endoscopy 2013, 45 (Suppl. 2), E252–E253. [Google Scholar] [CrossRef] [PubMed]
- Zator, Z.; Klinge, M.; Schraut, W.; Tsung, A.; Khalid, A. One step endoscopic ultrasound guided management of pelvic abscesses: A case series. Therap. Adv. Gastroenterol. 2018, 11, 1756284818785574. [Google Scholar] [CrossRef]
- Simons-Linares, C.R.; Chahal, P. Successful EUS-guided Drainage of a Persistent Subdiaphragmatic Fluid Collection in a Patient with Crohn’s Disease. Inflamm. Bowel Dis. 2019, 25, e85–e86. [Google Scholar] [CrossRef] [PubMed]
- Khalid, A.; Faisal, M.F. Endoscopic Ultrasound-Guided Transrectal Drainage of Perirectal Abscess in a Patient with Crohn Disease. Am. J. Case Rep. 2021, 22, e930698. [Google Scholar] [CrossRef]
- Monino, L.; Gonzalez, J.M.; Serrero, M.; Barthet, M. First case of endoscopic ultrasound-guided gastrojejunal anastomosis for duodenal stricture in refractory Crohn’s disease: A bridge toward inflammation control. Endoscopy 2020, 52, E204–E205. [Google Scholar] [CrossRef]
- Fusaroli, P.; Saftoiu, A.; Mancino, M.G.; Caletti, G.; Eloubeidi, M.A. Techniques of image enhancement in EUS (with videos). Gastrointest. Endosc. 2011, 74, 645–655. [Google Scholar] [CrossRef]
- Fuccio, L.; Attili, F.; Larghi, A. Forward-viewing linear echoendoscope: A new option in the endoscopic ultrasound armamentarium (with video). J. Hepatobiliary Pancreat. Sci. 2015, 22, 27–34. [Google Scholar] [CrossRef] [PubMed]
- Larghi, A.; Ibrahim, M.; Fuccio, L.; Lekkerkerker, S.; Eisendrath, P.; Frazzoni, L.; Fockens, P.; La Marca, M.; van Hooft, J.E.; Deviere, J.; et al. Forward-viewing echoendoscope versus standard echoendoscope for endoscopic ultrasound-guided tissue acquisition of solid lesions: A randomized, multicenter study. Endoscopy 2019, 51, 444–451. [Google Scholar] [CrossRef]
- LeBlanc, J.K. An overview of endoscopic ultrasound equipment. Minerva Gastroenterol. Dietol. 2008, 54, 177–187. [Google Scholar] [PubMed]
- Seifert, H.; Fusaroli, P.; Arcidiacono, P.G.; Braden, B.; Herth, F.; Hocke, M.; Larghi, A.; Napoleon, B.; Rimbas, M.; Ungureanu, B.S.; et al. Controversies in EUS: Do we need miniprobes? Endosc. Ultrasound. 2021, 10, 246–269. [Google Scholar] [PubMed]
Component | Score |
---|---|
Bowel wall thickening | |
Normal ≤3.0 mm | 0 |
Mild thickening 3.1–4.0 mm | 1 |
Moderate thickening 4.1–6.0 mm | 2 |
Severe thickening >6.0 mm | 3 |
Depth of inflammation | |
Superficial: No disruption of the 5-layer echo pattern | 0 |
Subepithelial: Disruption of the first 3 layers to the submucosa but not beyond | 1 |
Deep: Disruption beyond the submucosa to the muscularis propria | 2 |
Transmural: Disruption beyond the muscularis propria to the serosa or beyond | 3 |
Hyperemia | |
Normal: Absence of intramural vascular signal | 0 |
Mild: Intermittent signal | 1 |
Moderate: Continuous signal | 2 |
Severe: Presence of intramural anechoic vessel seen without power Doppler, with immediate continuous signal on power Doppler | 3 |
TOTAL | 9 |
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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
Statie, R.-C.; Florescu, D.N.; Gheonea, D.-I.; Ungureanu, B.S.; Iordache, S.; Rogoveanu, I.; Ciurea, T. The Use of Endoscopic Ultrasonography in Inflammatory Bowel Disease: A Review of the Literature. Diagnostics 2023, 13, 568. https://doi.org/10.3390/diagnostics13030568
Statie R-C, Florescu DN, Gheonea D-I, Ungureanu BS, Iordache S, Rogoveanu I, Ciurea T. The Use of Endoscopic Ultrasonography in Inflammatory Bowel Disease: A Review of the Literature. Diagnostics. 2023; 13(3):568. https://doi.org/10.3390/diagnostics13030568
Chicago/Turabian StyleStatie, Răzvan-Cristian, Dan Nicolae Florescu, Dan-Ionuț Gheonea, Bogdan Silviu Ungureanu, Sevastița Iordache, Ion Rogoveanu, and Tudorel Ciurea. 2023. "The Use of Endoscopic Ultrasonography in Inflammatory Bowel Disease: A Review of the Literature" Diagnostics 13, no. 3: 568. https://doi.org/10.3390/diagnostics13030568
APA StyleStatie, R.-C., Florescu, D. N., Gheonea, D.-I., Ungureanu, B. S., Iordache, S., Rogoveanu, I., & Ciurea, T. (2023). The Use of Endoscopic Ultrasonography in Inflammatory Bowel Disease: A Review of the Literature. Diagnostics, 13(3), 568. https://doi.org/10.3390/diagnostics13030568