Intestinal Ultrasound in the Assessment of Luminal Crohn’s Disease
Abstract
:1. Introduction
2. Performing Intestinal Ultrasound
2.1. Patient Preparation
2.2. General Technique of Ultrasound
2.3. Enhancement Techniques
3. Findings and Accuracy of IUS in CD Activity Assessment
3.1. Accuracy in Small Bowel CD Activity Assessment
3.2. Bowel Wall Thickness
3.3. Doppler Vascularity
3.4. Inflammatory Mesenteric Fat and Lymphadenopathy
3.5. Peristalsis
3.6. Strictures
3.7. Enteric Fistula and Abscess Detection
4. IUS Indices
5. Response to Therapy and Monitoring
6. Postoperative Recurrence
7. Novel Areas of Utility
7.1. Sonoelastography
7.2. Pregnancy
8. Limitations of IUS
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ng, S.C.; Shi, H.Y.; Hamidi, N.; Underwood, F.E.; Tang, W.; Benchimol, E.I.; Panaccione, R.; Ghosh, S.; Wu, J.C.Y.; Chan, F.K.L.; et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: A systematic review of population-based studies. Lancet 2017, 390, 2769–2778. [Google Scholar] [CrossRef]
- Chouraki, V.; Savoye, G.; Dauchet, L.; Vernier-Massouille, G.; Dupas, J.-L.; Merle, V.; Laberenne, J.-E.; Salomez, J.-L.; Lerebours, E.; Turck, D.; et al. The changing pattern of Crohn’s disease incidence in northern France: A continuing increase in the 10- to 19-year-old age bracket (1988–2007). Aliment. Pharmacol. Ther. 2011, 33, 1133–1142. [Google Scholar] [CrossRef] [PubMed]
- Maaser, C.; Sturm, A.; Vavricka, S.R.; Kucharzik, T.; Fiorino, G.; Annese, V.; Calabrese, E.; Baumgart, D.C.; Bettenworth, D.; Borralho Nunes, P.; et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. J. Crohn’s Colitis 2018, 13, 144–164K. [Google Scholar] [CrossRef]
- Turner, D.; Ricciuto, A.; Lewis, A.; D’Amico, F.; Dhaliwal, J.; Griffiths, A.M.; Bettenworth, D.; Sandborn, W.J.; Sands, B.E.; Reinisch, W.; et al. STRIDE-II: An Update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) Initiative of the International Organization for the Study of IBD (IOIBD): Determining Therapeutic Goals for Treat-to-Target strategies in IBD. Gastroenterology 2021, 160, 1570–1583. [Google Scholar] [CrossRef] [PubMed]
- Bryant, R.V.; Friedman, A.B.; Wright, E.K.; Taylor, K.M.; Begun, J.; Maconi, G.; Maaser, C.; Novak, K.L.; Kucharzik, T.; Atkinson, N.S.S.; et al. Gastrointestinal ultrasound in inflammatory bowel disease: An underused resource with potential paradigm-changing application. Gut 2018, 67, 973–985. [Google Scholar] [CrossRef] [PubMed]
- Hata, J.; Imamura, H. The Use of Transabdominal Ultrasound in Inflammatory Bowel Disease. Korean J. Radiol. 2022, 23, 308–321. [Google Scholar] [CrossRef]
- Rajagopalan, A.; Sathananthan, D.; An, Y.; Van De Ven, L.; Martin, S.; Fon, J.; Costello, S.P.; Begun, J.; Bryant, R.V. Gastrointestinal ultrasound in inflammatory bowel disease care: Patient perceptions and impact on disease-related knowledge. JGH Open 2019, 4, 267–272. [Google Scholar] [CrossRef]
- Friedman, A.B.; Asthana, A.; Knowles, S.R.; Robbins, A.; Gibson, P.R. Effect of point-of-care gastrointestinal ultrasound on decision-making and management in inflammatory bowel disease. Aliment. Pharmacol. Ther. 2021, 54, 652–666. [Google Scholar] [CrossRef]
- Novak, K.; Tanyingoh, D.; Petersen, F.; Kucharzik, T.; Panaccione, R.; Ghosh, S.; Kaplan, G.G.; Wilson, A.; Kannengiesser, K.; Maaser, C. Clinic-based Point of Care Transabdominal Ultrasound for Monitoring Crohn’s Disease: Impact on Clinical Decision Making. J. Crohn’s Colitis 2015, 9, 795–801. [Google Scholar] [CrossRef]
- Wright, E.K.; Wang, I.; Wong, D.; Bell, S.J.; Connell, W.R.; Thompson, A.J.; Novak, K.L.; Kamm, M.A. Accuracy of point-of-care intestinal ultrasound for Crohn’s disease. Australas. J. Ultrasound Med. 2020, 23, 176–182. [Google Scholar] [CrossRef]
- Bots, S.; De Voogd, F.; De Jong, M.; Ligtvoet, V.; Löwenberg, M.; Duijvestein, M.; Ponsioen, C.Y.; D’Haens, G.; Gecse, K.B. Point-of-care Intestinal Ultrasound in IBD Patients: Disease Management and Diagnostic Yield in a Real-world Cohort and Proposal of a Point-of-care Algorithm. J. Crohn’s Colitis 2021, 16, 606–615. [Google Scholar] [CrossRef]
- Panes, J.; Bouhnik, Y.; Reinisch, W.; Stoker, J.; Taylor, S.; Baumgart, D.; Danese, S.; Halligan, S.; Marincek, B.; Matos, C.; et al. Imaging techniques for assessment of inflammatory bowel disease: Joint ECCO and ESGAR evidence-based consensus guidelines. J. Crohn’s Colitis 2013, 7, 556–585. [Google Scholar] [CrossRef] [PubMed]
- Atkinson, N.S.S.; Bryant, R.V.; Dong, Y.; Maaser, C.; Kucharzik, T.; Maconi, G.; Asthana, A.K.; Blaivas, M.; Goudie, A.; Gilja, O.H.; et al. How to perform gastrointestinal ultrasound: Anatomy and normal findings. World J. Gastroenterol. 2017, 23, 6931–6941. [Google Scholar] [CrossRef] [PubMed]
- Sinan, T.; Leven, H.; Sheikh, M. Is fasting a necessary preparation for abdominal ultrasound? BMC Med. Imaging 2003, 3, 1. [Google Scholar] [CrossRef] [PubMed]
- Ehrenstein, B.P.; Froh, S.; Schlottmann, K.; Schölmerich, J.; Schacherer, D. To eat or not to eat? Effect of fasting prior to abdominal sonography examinations on the quality of imaging under routine conditions: A randomized, examiner-blinded trial. Scand. J. Gastroenterol. 2009, 44, 1048–1054. [Google Scholar] [CrossRef]
- Nylund, K.; Maconi, G.; Hollerweger, A.; Ripolles, T.; Pallotta, N.; Higginson, A.; Serra, C.; Dietrich, C.F.; Sporea, I.; Saftoiu, A.; et al. EFSUMB Recommendations and Guidelines for Gastrointestinal Ultrasound-Part 1: Examination Techniques and Normal Findings (Short version). Ultraschall der Med.-Eur. J. Ultrasound 2016, 38, 273–284. [Google Scholar] [CrossRef]
- Parente, F.; Greco, S.; Molteni, M.; Anderloni, A.; Sampietro, G.M.; Danelli, P.; Bianco, R.; Gallus, S.; Porro, G.B. Oral contrast enhanced bowel ultrasonography in the assessment of small intestine Crohn’s disease. A prospective comparison with conventional ultrasound, x ray studies, and ileocolonoscopy. Gut 2004, 53, 1652–1657. [Google Scholar] [CrossRef]
- Ripollés, T.; Martínez-Pérez, M.J.; Paredes, J.M.; Vizuete, J.; García-Martínez, E.; Jiménez-Restrepo, D.H. Contrast-enhanced ultrasound in the differentiation between phlegmon and abscess in Crohn’s disease and other abdominal conditions. Eur. J. Radiol. 2013, 82, e525–e531. [Google Scholar] [CrossRef]
- Medellin, A.; Merrill, C.; Wilson, S.R. Role of contrast-enhanced ultrasound in evaluation of the bowel. Abdom. Radiol. 2017, 43, 918–933. [Google Scholar] [CrossRef]
- Mocci, G.; Migaleddu, V.; Cabras, F.; Sirigu, D.; Scanu, D.; Virgilio, G.; Marzo, M. SICUS and CEUS imaging in Crohn’s disease: An update. J. Ultrasound 2017, 20, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Ripollés, T.; Martínez-Pérez, M.J.; Blanc, E.; Delgado, F.; Vizuete, J.; Paredes, J.M.; Vilar, J. Contrast-enhanced ultrasound (CEUS) in Crohn’s disease: Technique, image interpretation and clinical applications. Insights Into Imaging 2011, 2, 639–652. [Google Scholar] [CrossRef] [PubMed]
- A Taylor, S.; Mallett, S.; Bhatnagar, G.; Baldwin-Cleland, R.; Bloom, S.; Gupta, A.; Hamlin, P.J.; Hart, A.L.; Higginson, A.; Jacobs, I.; et al. Diagnostic accuracy of magnetic resonance enterography and small bowel ultrasound for the extent and activity of newly diagnosed and relapsed Crohn’s disease (METRIC): A multicentre trial. Lancet Gastroenterol. Hepatol. 2018, 3, 548–558. [Google Scholar] [CrossRef]
- Calabrese, E.; Maaser, C.; Zorzi, F.; Kannengiesser, K.; Hanauer, S.B.; Bruining, D.H.; Iacucci, M.; Maconi, G.; Novak, K.L.; Panaccione, R.; et al. Bowel Ultrasonography in the Management of Crohn’s Disease. A Review with Recommendations of an International Panel of Experts. Inflamm. Bowel Dis. 2016, 22, 1168–1183. [Google Scholar] [CrossRef]
- Maconi, G.; Nylund, K.; Ripolles, T.; Calabrese, E.; Dirks, K.; Dietrich, C.F.; Hollerweger, A.; Sporea, I.; Saftoiu, A.; Maaser, C.; et al. EFSUMB Recommendations and Clinical Guidelines for Intestinal Ultrasound (GIUS) in Inflammatory Bowel Diseases. Ultraschall der Med.-Eur. J. Ultrasound 2018, 39, 304–317. [Google Scholar] [CrossRef]
- Dong, J.; Wang, H.; Zhao, J.; Zhu, W.; Zhang, L.; Gong, J.; Li, Y.; Gu, L.; Li, J. Ultrasound as a diagnostic tool in detecting active Crohn’s disease: A meta-analysis of prospective studies. Eur. Radiol. 2013, 24, 26–33. [Google Scholar] [CrossRef] [PubMed]
- Sævik, F.; Eriksen, R.; Eide, G.E.; Gilja, O.H.; Nylund, K. Development and Validation of a Simple Ultrasound Activity Score for Crohn’s Disease. J. Crohn’s Colitis 2020, 15, 115–124. [Google Scholar] [CrossRef] [PubMed]
- Maconi, G.; Carsana, L.; Fociani, P.; Sampietro, G.M.; Ardizzone, S.; Cristaldi, M.; Parente, F.; Vago, G.L.; Taschieri, A.M.; Porro, G.B. Small bowel stenosis in Crohn’s disease: Clinical, biochemical and ultrasonographic evaluation of histological features. Aliment. Pharmacol. Ther. 2003, 18, 749–756. [Google Scholar] [CrossRef] [PubMed]
- Rigazio, C.; Ercole, E.; Laudi, C.; Daperno, M.; Lavagna, A.; Crocellà, L.; Bertolino, F.; Viganò, L.; Sostegni, R.; Pera, A.; et al. Abdominal bowel ultrasound can predict the risk of surgery in Crohn’s disease: Proposal of an ultrasonographic score. Scand. J. Gastroenterol. 2009, 44, 585–593. [Google Scholar] [CrossRef]
- Maconi, G.; Greco, S.; Duca, P.; Ardizzone, S.; Massari, A.; Cassinotti, A.; Radice, E.; Porro, G.B. Prevalence and clinical significance of sonographic evidence of mesenteric fat alterations in Crohn’s disease. Inflamm. Bowel Dis. 2008, 14, 1555–1561. [Google Scholar] [CrossRef]
- Novak, K.L.; Nylund, K.; Maaser, C.; Petersen, F.; Kucharzik, T.; Lu, C.; Allocca, M.; Maconi, G.; de Voogd, F.; Christensen, B.; et al. Expert Consensus on Optimal Acquisition and Development of the International Bowel Ultrasound Segmental Activity Score [IBUS-SAS]: A Reliability and Inter-rater Variability Study on Intestinal Ultrasonography in Crohn’s Disease. J. Crohn’s Colitis 2020, 15, 609–616. [Google Scholar] [CrossRef]
- Allocca, M.; Craviotto, V.; Dell’Avalle, C.; Furfaro, F.; Zilli, A.; D’Amico, F.; Bonovas, S.; Peyrin-Biroulet, L.; Fiorino, G.; Danese, S. Bowel ultrasound score is accurate in assessing response to therapy in patients with Crohn’s disease. Aliment. Pharmacol. Ther. 2021, 55, 446–454. [Google Scholar] [CrossRef] [PubMed]
- Allocca, M.; Craviotto, V.; Bonovas, S.; Furfaro, F.; Zilli, A.; Peyrin-Biroulet, L.; Fiorino, G.; Danese, S. Predictive Value of Bowel Ultrasound in Crohn’s Disease: A 12-Month Prospective Study. Clin. Gastroenterol. Hepatol. 2021, 20, e723–e740. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Ding, S.-S.; Zhang, K.; Liu, L.-N.; Guo, L.-H.; Sun, L.-P.; Zhang, Y.-F.; Sun, X.-M.; Ren, W.-W.; Zhao, C.-K.; et al. Correlation between ultrasound consolidated score and simple endoscopic score for determining the activity of Crohn’s disease. Br. J. Radiol. 2020, 93, 20190614. [Google Scholar] [CrossRef] [PubMed]
- Novak, K.L.; Kaplan, G.G.; Panaccione, R.; Afshar, E.E.; Tanyingoh, D.; Swain, M.; Kellar, A.; Wilson, S. A Simple Ultrasound Score for the Accurate Detection of Inflammatory Activity in Crohn’s Disease. Inflamm. Bowel Dis. 2017, 23, 2001–2010. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, T.; Kunisaki, R.; Kinoshita, H.; Yamamoto, H.; Kimura, H.; Hanzawa, A.; Shibata, N.; Yonezawa, H.; Miyajima, E.; Sakamaki, K.; et al. Use of color Doppler ultrasonography for evaluating vascularity of small intestinal lesions in Crohn’s disease: Correlation with endoscopic and surgical macroscopic findings. Scand. J. Gastroenterol. 2013, 49, 295–301. [Google Scholar] [CrossRef] [PubMed]
- Drews, B.H.; Barth, T.F.E.; Hänle, M.M.; Akinli, A.S.; Mason, R.A.; Muche, R.; Thiel, R.; Pauls, S.; Klaus, J.; Von Boyen, G.; et al. Comparison of sonographically measured bowel wall vascularity, histology, and disease activity in Crohn’s disease. Eur. Radiol. 2009, 19, 1379–1386. [Google Scholar] [CrossRef]
- Pascu, M.; Roznowski, A.B.; Müller, H.-P.; Adler, A.; Wiedenmann, B.; Dignass, A.U. Clinical Relevance of Transabdominal Ultrasonography and Magnetic Resonance Imaging in Patients With Inflammatory Bowel Disease of the Terminal Ileum and Large Bowel. Inflamm. Bowel Dis. 2004, 10, 373–382. [Google Scholar] [CrossRef]
- Neye, H.; Voderholzer, W.; Rickes, S.; Weber, J.; Wermke, W.; Lochs, H. Evaluation of Criteria for the Activity of Crohn’s Disease by Power Doppler Sonography. Dig. Dis. 2004, 22, 67–72. [Google Scholar] [CrossRef]
- Jauregui-Amezaga, A.; Rimola, J. Role of Intestinal Ultrasound in the Management of Patients with Inflammatory Bowel Disease. Life 2021, 11, 603. [Google Scholar] [CrossRef]
- Bettenworth, D.; Bokemeyer, A.; Baker, M.; Mao, R.; Parker, C.E.; Nguyen, T.; Ma, C.; Panés, J.; Rimola, J.; Fletcher, J.G.; et al. Assessment of Crohn’s disease-associated small bowel strictures and fibrosis on cross-sectional imaging: A systematic review. Gut 2019, 68, 1115–1126. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.; Hakim, A.; Alexakis, C.; Chhaya, V.; Tzias, D.; Pilcher, J.; Vlahos, J.; Pollok, R. Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn’s disease: Correlation with intraoperative findings and magnetic resonance enterography. J. Gastroenterol. Hepatol. 2014, 30, 86–91. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Jiang, W.; Wang, L.; Mao, X.; Ye, Z.; Zhang, H. Intestinal Ultrasound for Differentiating Fibrotic or Inflammatory Stenosis in Crohn’s Disease: A Systematic Review and Meta-analysis. J. Crohn’s Colitis 2022, 30, 86–91. [Google Scholar] [CrossRef] [PubMed]
- Panes, J.; Bouzas, R.; Chaparro, M.; García-Sánchez, V.; Gisbert, J.P.; De Guereñu, B.M.; Mendoza, J.L.; Paredes, J.M.; Quiroga, S.; Ripollés, T.; et al. Systematic review: The use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment. Pharmacol. Ther. 2011, 34, 125–145. [Google Scholar] [CrossRef] [PubMed]
- Goodsall, T.M.; Nguyen, T.M.; Parker, C.E.; Ma, C.; Andrews, J.M.; Jairath, V.; Bryant, R.V. Systematic Review: Gastrointestinal Ultrasound Scoring Indices for Inflammatory Bowel Disease. J. Crohn’s Colitis 2020, 15, 125–142. [Google Scholar] [CrossRef] [PubMed]
- Bots, S.; Nylund, K.; Löwenberg, M.; Gecse, K.; Gilja, O.H.; D’Haens, G. Ultrasound for Assessing Disease Activity in IBD Patients: A Systematic Review of Activity Scores. J. Crohn’s Colitis 2018, 12, 920–929. [Google Scholar] [CrossRef]
- Goodsall, T.M.; Jairath, V.; Feagan, B.G.; Parker, C.E.; Nguyen, T.M.; Guizzetti, L.; Asthana, A.K.; Begun, J.; Christensen, B.; Friedman, A.B.; et al. Standardisation of intestinal ultrasound scoring in clinical trials for luminal Crohn’s disease. Aliment. Pharmacol. Ther. 2021, 53, 873–886. [Google Scholar] [CrossRef]
- Calabrese, E.; Rispo, A.; Zorzi, F.; De Cristofaro, E.; Testa, A.; Costantino, G.; Viola, A.; Bezzio, C.; Ricci, C.; Prencipe, S.; et al. Ultrasonography Tight Control and Monitoring in Crohn’s Disease During Different Biological Therapies: A Multicenter Study. Clin. Gastroenterol. Hepatol. 2021, 20, e711–e722. [Google Scholar] [CrossRef]
- Ilvemark, J.F.K.F.; Hansen, T.; Goodsall, T.M.; Seidelin, J.B.; Farhan, H.A.; Allocca, M.; Begun, J.; Bryant, R.V.; Carter, D.; Christensen, B.; et al. Defining Transabdominal Intestinal Ultrasound Treatment Response and Remission in Inflammatory Bowel Disease: Systematic Review and Expert Consensus Statement. J. Crohn’s Colitis 2021, 16, 554–580. [Google Scholar] [CrossRef]
- Kucharzik, T.; Wittig, B.M.; Helwig, U.; Börner, N.; Rössler, A.; Rath, S.; Maaser, C.; Naumann, A.; Pelster, G.; Spengler, J.; et al. Use of Intestinal Ultrasound to Monitor Crohn’s Disease Activity. Clin. Gastroenterol. Hepatol. 2016, 15, 535–542.e2. [Google Scholar] [CrossRef]
- Ripollés, T.; Paredes, J.M.; Martínez-Pérez, M.J.; Rimola, J.; Jauregui-Amezaga, A.; Bouzas, R.; Martin, G.; Moreno-Osset, E. Ultrasonographic Changes at 12 Weeks of Anti-TNF Drugs Predict 1-year Sonographic Response and Clinical Outcome in Crohn’s Disease. Inflamm. Bowel Dis. 2016, 22, 2465–2473. [Google Scholar] [CrossRef]
- Castiglione, F.; Testa, A.; Rea, M.; De Palma, G.D.; Diaferia, M.; Musto, D.; Sasso, F.; Caporaso, N.; Rispo, A. Transmural Healing Evaluated by Bowel Sonography in Patients with Crohn’s Disease on Maintenance Treatment with Biologics. Inflamm. Bowel Dis. 2013, 19, 1928–1934. [Google Scholar] [CrossRef] [PubMed]
- Ma, L.; Li, W.; Zhuang, N.; Yang, H.; Liu, W.; Zhou, W.; Jiang, Y.; Li, J.; Zhu, Q.; Qian, J. Comparison of transmural healing and mucosal healing as predictors of positive long-term outcomes in Crohn’s disease. Ther. Adv. Gastroenterol. 2021, 14. [Google Scholar] [CrossRef] [PubMed]
- Zorzi, F.; Ghosh, S.; Chiaramonte, C.; Lolli, E.; Ventura, M.; Onali, S.; De Cristofaro, E.; Fantini, M.C.; Biancone, L.; Monteleone, G.; et al. Response Assessed by Ultrasonography as Target of Biological Treatment for Crohn’s Disease. Clin. Gastroenterol. Hepatol. 2020, 18, 2030–2037. [Google Scholar] [CrossRef] [PubMed]
- Moreno, N.; Ripollés, T.; Paredes, J.M.; Ortiz, I.; Martínez, M.J.; López, A.; Delgado, F.; Moreno-Osset, E. Usefulness of abdominal ultrasonography in the analysis of endoscopic activity in patients with Crohn’s disease: Changes following treatment with immunomodulators and/or anti-TNF antibodies. J. Crohn’s Colitis 2014, 8, 1079–1087. [Google Scholar] [CrossRef] [PubMed]
- Laterza, L.; Ainora, M.E.; Garcovich, M.; Galasso, L.; Poscia, A.; Di Stasio, E.; Lupascu, A.; Riccardi, L.; Scaldaferri, F.; Armuzzi, A.; et al. Bowel contrast-enhanced ultrasound perfusion imaging in the evaluation of Crohn’s disease patients undergoing anti-TNFα therapy. Dig. Liver Dis. 2020, 53, 729–737. [Google Scholar] [CrossRef] [PubMed]
- Vaughan, R.; Tjandra, D.; Patwardhan, A.; Mingos, N.; Gibson, R.; Boussioutas, A.; Ardalan, Z.; Al-Ani, A.; Gibson, P.R.; Christensen, B. Toward transmural healing: Sonographic healing is associated with improved long-term outcomes in patients with Crohn’s disease. Aliment. Pharmacol. Ther. 2022, 56, 84–94. [Google Scholar] [CrossRef]
- Macedo, C.P.; Costa, M.S.; Gravito-Soares, E.; Gravito-Soares, M.; Ferreira, A.M.; Portela, F.; Figueiredo, P. Role of Intestinal Ultrasound in the Evaluation of Postsurgical Recurrence in Crohn’s Disease: Correlation with Endoscopic Findings. GE-Port. J. Gastroenterol. 2021, 29, 178–186. [Google Scholar] [CrossRef]
- Calabrese, E.; Petruzziello, C.; Onali, S.; Condino, G.; Zorzi, F.; Pallone, F.; Biancone, L. Severity of postoperative recurrence in Crohn’s disease: Correlation between endoscopic and sonographic findings. Inflamm. Bowel Dis. 2009, 15, 1635–1642. [Google Scholar] [CrossRef]
- Rispo, A.; Bucci, L.; Pesce, G.; Sabbatini, F.; De Palma, G.D.; Grassia, R.; Compagna, A.; Testa, A.; Castiglione, F. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm. Bowel Dis. 2006, 12, 486–490. [Google Scholar] [CrossRef]
- Rispo, A.; Imperatore, N.; Testa, A.; Nardone, O.M.; Luglio, G.; Caporaso, N.; Castiglione, F. Diagnostic Accuracy of Ultrasonography in the Detection of Postsurgical Recurrence in Crohn’s Disease: A Systematic Review with Meta-analysis. Inflamm. Bowel Dis. 2018, 24, 977–988. [Google Scholar] [CrossRef]
- Martínez, M.J.; Ripollés, T.; Paredes, J.M.; Moreno-Osset, E.; Pazos, J.M.; Blanc, E. Intravenous Contrast-Enhanced Ultrasound for Assessing and Grading Postoperative Recurrence of Crohn’s Disease. Am. J. Dig. Dis. 2019, 64, 1640–1650. [Google Scholar] [CrossRef] [PubMed]
- Paredes, J.M.; Ripollés, T.; Cortés, X.; Moreno, N.; Martínez, M.J.; Bustamante-Balén, M.; Delgado, F.; Moreno-Osset, E. Contrast-enhanced ultrasonography: Usefulness in the assessment of postoperative recurrence of Crohn’s disease. J. Crohn’s Colitis 2013, 7, 192–201. [Google Scholar] [CrossRef] [PubMed]
- Castiglione, F.; Bucci, L.; Pesce, G.; De Palma, G.D.; Camera, L.; Cipolletta, F.; Testa, A.; Diaferia, M.; Rispo, A. Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm. Bowel Dis. 2008, 14, 1240–1245. [Google Scholar] [CrossRef] [PubMed]
- Herraiz Hidalgo, L.; Alvarez Moreno, E.; Carrascoso Arranz, J.; Cano Alonso, R.; de Vega Fernández, V.M. Magnetic resonance enterography: Review of the technique for the study of Crohn’s disease. Radiologia 2011, 53, 421–433. [Google Scholar] [CrossRef]
- Vestito, A.; Marasco, G.; Maconi, G.; Festi, D.; Bazzoli, F.; Zagari, R.M. Role of Ultrasound Elastography in the Detection of Fibrotic Bowel Strictures in Patients with Crohn’s Disease: Systematic Review and Meta-Analysis. Ultraschall der Med.-Eur. J. Ultrasound 2019, 40, 646–654. [Google Scholar] [CrossRef]
- Fraquelli, M.; Branchi, F.; Cribiù, F.M.; Orlando, S.; Casazza, G.; Magarotto, A.; Massironi, S.; Botti, F.; Contessini-Avesani, E.; Conte, D.; et al. The Role of Ultrasound Elasticity Imaging in Predicting Ileal Fibrosis in Crohn’s Disease Patients. Inflamm. Bowel Dis. 2015, 21, 2605–2612. [Google Scholar] [CrossRef]
- Chen, Y.-J.; Mao, R.; Li, X.-H.; Cao, Q.-H.; Chen, Z.-H.; Liu, B.-X.; Chen, S.-L.; Chen, B.-L.; He, Y.; Zeng, Z.-R.; et al. Real-Time Shear Wave Ultrasound Elastography Differentiates Fibrotic from Inflammatory Strictures in Patients with Crohn’s Disease. Inflamm. Bowel Dis. 2018, 24, 2183–2190. [Google Scholar] [CrossRef]
- De Voogd, F.; Joshi, H.; Van Wassenaer, E.; Bots, S.; D’Haens, G.; Gecse, K. Intestinal Ultrasound to Evaluate Treatment Response During Pregnancy in Patients with Inflammatory Bowel Disease. Inflamm. Bowel Dis. 2021, 28, 1045–1052. [Google Scholar] [CrossRef]
- Flanagan, E.; Wright, E.K.; Begun, J.; Bryant, R.V.; An, Y.-K.; Ross, A.L.; Kiburg, K.V.; Bell, S.J. Monitoring Inflammatory Bowel Disease in Pregnancy Using Gastrointestinal Ultrasonography. J. Crohn’s Colitis 2020, 14, 1405–1412. [Google Scholar] [CrossRef]
- Leung, Y.; Shim, H.H.; Wilkens, R.; Tanyingoh, D.; Afshar, E.E.; Sharifi, N.; Pauls, M.; Novak, K.L.; Kaplan, G.G.; Panaccione, R.; et al. The Role of Bowel Ultrasound in Detecting Subclinical Inflammation in Pregnant Women with Crohn’s Disease. J. Can. Assoc. Gastroenterol. 2018, 2, 153–160. [Google Scholar] [CrossRef]
- Asthana, A.K.; Friedman, A.B.; Maconi, G.; Maaser, C.; Kucharzik, T.; Watanabe, M.; Gibson, P.R. The failure of gastroenterologists to apply intestinal ultrasound in inflammatory bowel disease in the Asia-Pacific: A need for action. J. Gastroenterol. Hepatol. 2014, 30, 446–452. [Google Scholar] [CrossRef] [PubMed]
Stricture | Narrowing of the lumen (diameter < 1 cm) with associated thickening of the regional bowel wall (>3 mm). May be associated with prestenotic dilatation (lumen diameter > 30 mm) with hyper peristalsis in the bowel proximal to the stricture. |
Fistula | Hypoechoic areas or tracts between ileal loops with or without internal gaseous artifacts. Hypoechoic peri-intestinal tracts with or without gas within. Hypoechoic peri-intestinal areas with a diameter < 2 cm. |
Abscess | Hypoanechoic lesions containing fluid and gaseous artifacts. May be associated with posterior enhancement and irregular margins sometimes within hypertrophic mesentery |
Grade | Parameter |
---|---|
0 | No bowel wall thickening ≤ 4 mm, no vascularisation |
1 | Bowel wall thickening > 4 mm, no vascularisation |
2 | Bowel wall thickening > 4 mm with short stretches of vascularity |
3 | Bowel wall thickening > 4 mm with long stretches of vascularity |
4 | Bowel wall thickening > 4 mm with long stretches of vascularity reaching into the mesentery |
Index | Study Design | n | Reference Index | Included Parameters | Segment Assessed | Formula | Power | Fasting/Contrast | |
---|---|---|---|---|---|---|---|---|---|
Allocca 2021 [31,32] | BUSS | P | 225 | Colonoscopy (SES-CD) | BWT BWF | I C AC TC DC SC Rec | BUSS = 0.75 × BWT + 1.65 × BWF | BUSS >3.52 defined active disease Sensitivity 83% (95% CI, 76–88%) Specificity 85% (95% CI, 73–93%) AuROC of 0.86 (95% CI, 0.81–0.91) | Nil/Nil |
Novak 2021 [30] | IBUS-SAS | P | N/A | N/A | BWT ifat CDS BWS | PSB I TI AC AC TC DC SC | IBUS−SAS = 4 × BWT + 15 × i-fat + 7 × CDS + 4 × BWS | Score 0−100 Validation study in progress | Nil/Nil |
Liu 2020 [33] | UCS | R | 66 | Colonoscopy (SES-CD) | Symmetry Echogenicity of the peribowel fat Limberg score Echogenicity of the bowel wall BWT | TI RC TC LC | UCS = S1 (score for symmetry) + S2 (score for the echogenicity of peribowel fat) + S3 (Limberg score) + S4 (score for bowel wall layer structure) + S5 (score for the echogenicity of the bowel walls) + S6 (score for BWT) | UCS >6 defined active disease AuROC of 0.98 Sensitivity 88% Specificity 96% PPV 94% NPV 91% Accuracy 92%, Correlation coefficient between UCS and SES: 0.90 | 8 h/1000 mL of 2.5% isotonic mannitol |
Sævik 2020 [26] | SUS-CD | P | P1-40 P2-124 | Colonoscopy (SES-CD) | BWT CDS | TI RC TC LC Rec | SUS-CD = BWT + CDS | SUS-CD to predict active endoscopic disease AuROC of 0.92 Sensitivity 95% Specificity 70% | Nil/Nil |
Novak 2017 [34] | SSS | P1-R P2-P | P1-160 P1-63 | Colonoscopy (SES-CD) | BWT CDS | I C AC TC DC Rec | SSS = [0.0563 × BWT1] + [2.0047 × BWT2] + [3.0881 × BWT3] + [1.0204 × CDS1] + [1.5460 × CDS2] | SSS to predict active/inactive endoscopic disease AuROC (P1) of 0.87 AuROC (P2) of 0.84 | 8 h/Nil |
Sasaki 2014 [35] | LS | R | C-108 Histology-22 | C(SES-CD) Histology specimen | BWT CDS | TI | Limberg score | Endoscopy: correlation coefficient of r = 0.709 (p < 0.001). Sensitivity: 39% Specificity 100% Accuracy 61% Histological specimen Sensitivity: 65% Specificity: 100% Accuracy: 73% | nil/nil |
Drews 2009 [36] | LS | R | 31 | Histology specimen | BWT CDS | TI | Limberg score | κ = 0.66 (p < 0.05) Sensitivity 95% Specificity 69% | Nil/nil |
Pascu 2004 [37] | PAS | P | 61 | Colonoscopy | BWT BWS CDI Loss of compressibility | TI C AC TC DC SC Rec ANC | Categorical and sum per segment score 0 = BWT <3 mm and no CDI 1 = BWT 3–5 mm with increased CDI, loss of compressibility and persevered BWS 2 = BWT 5–8 mm, increased CDI, loss of compressibility, washed out BWS 3 = BWT >8 mm, increased CDI, loss of compressibility of BWS, peritoneal surface thickening | Endoscopic activity index correlated significantly with the US activity index (r = 0.884, p < 0.001) For CD Sensitivity 74% Specificity 97% PPV: 96% NPV: 79% | Nil/nil |
Neye 2004 [38] | NYS | P | 22 | Colonoscopy | BWT CDS | I TI C AC TC DC SC | NYS(Segmental) = BWT + CDS NYS(global) = sum of all segments | Per segment κ = 0.75(0.56–0.94)—0.91(0.83–0.98) | Nil/nil |
Maconi 2003 [27] | MS | P | 43 | Histology specimen | BWT BWS | UK | Grading: pathological bowel wall thickness with loss of stratification (hypoechoic echo pattern) pathological bowel wall thickness with stratification (stratified echo pattern) co-existence of tracts with/without stratification (mixed echo pattern) | Grading predicted histological stenosis: Sensitivity 100% Specificity 63% PPV 72% NPV 100% | Nil/nil |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Bohra, A.; Van Langenberg, D.R.; Vasudevan, A. Intestinal Ultrasound in the Assessment of Luminal Crohn’s Disease. Gastrointest. Disord. 2022, 4, 249-262. https://doi.org/10.3390/gidisord4040024
Bohra A, Van Langenberg DR, Vasudevan A. Intestinal Ultrasound in the Assessment of Luminal Crohn’s Disease. Gastrointestinal Disorders. 2022; 4(4):249-262. https://doi.org/10.3390/gidisord4040024
Chicago/Turabian StyleBohra, Anuj, Daniel R. Van Langenberg, and Abhinav Vasudevan. 2022. "Intestinal Ultrasound in the Assessment of Luminal Crohn’s Disease" Gastrointestinal Disorders 4, no. 4: 249-262. https://doi.org/10.3390/gidisord4040024
APA StyleBohra, A., Van Langenberg, D. R., & Vasudevan, A. (2022). Intestinal Ultrasound in the Assessment of Luminal Crohn’s Disease. Gastrointestinal Disorders, 4(4), 249-262. https://doi.org/10.3390/gidisord4040024