Abstract
Endoscopy remains the main technique in the diagnosis and treatment of Crohn’s disease (CD); nevertheless, the recent development of innovative and non-invasive imaging techniques has led to a new tool in the exploration of small bowel in CD patients. This paper reviews the available data on ultrasound imaging used for the evaluation of CD, highlighting the role of small intestine contrast-enhanced ultrasonography with the use of oral and intravenous contrast agents.
Sommario
Nell’iter diagnostico e terapeutico della malattia di Crohn l’endoscopia rappresenta la principale metodica strumentale. Tuttavia, la recente introduzione di tecniche di imaging innovative e non invasive ha implementato lo studio dell’intestino nelle malattie infiammatorie croniche intestinali. La seguente revisione raccoglie i dati disponibili in letteratura relativi all’utilizzo dell’ecografia con mezzo di contrasto, sia orale (SICUS) sia endovenoso (CEUS), nella valutazione dei pazienti affetti da malattia di Crohn.
Similar content being viewed by others
References
Cosnes J, Cattan S, Blain A et al (2002) Long-term evolution of disease behavior of Crohn’s disease. Inflamm Bowel Dis 8:244–250
Van Assche G, Dignass A, Reinisch W et al (2010) European Crohn’s and Colitis Organisation (ECCO). The second European evidence-based consensus on the diagnosis and management of Crohn’s disease: special situations. J Crohns Colitis 4:63–101
Van Assche G, Dignass A, Panes J et al (2010) European Crohn’s and Colitis Organisation (ECCO). The second European evidence-based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. J Crohns Colitis 4:7–27
Fletcher JG, Fidler JL, Bruining DH et al (2011) New concepts in intestinal imaging for inflammatory bowel diseases. Gastroenterology 140:1795–1806
Pariente B, Cosnes J, Danese S et al (2011) Development of the Crohn’s disease digestive damage score, the Lémann score. Inflamm Bowel Dis 17:1415–1422
Panés J, Bouzas R, Chaparro M et al (2011) 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 34:125–145
Horsthuis K, Bipat S, Bennink RJ et al (2008) Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology 247:64–79
Lichtenstein GR, Hanauer SB, Sandborn WJ (2009) Practice parameters committee of american college of gastroenterology. management of crohn’s disease in adults. Am J Gastroenterol 104:465–483
Panes J, Bouhnik Y, Reinisch W et al (2013) Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis 7:556–585
Jaffe TA, Gaca AM, Delaney S et al (2007) Radiation doses from small-bowel follow-through and abdominopelvic MDCT in Crohn’s disease. AJR Am J Roentgenol 189:1015–1022
Desmond AN, O’Regan K, Curran C et al (2008) Crohn’s disease: factors associated with exposure to high levels of diagnostic radiation. Gut 57:1524–1529
Valette PJ, Rioux M, Pilleul F et al (2001) Ultrasonography of chronic inflammatory bowel diseases. Eur Radiol 11:1859–1866
Calabrese E, Zorzi F, Pallone F (2012) Ultrasound of the small bowel in Crohn’s disease. Int J Inflam 2012:964720. doi:10.1155/2012/964720
Strobel D, Goertz RS, Bernatik T (2011) Diagnostics in inflammatory bowel disease: ultrasound. World J Gastroenterol 17:3192–3197
Maconi G, Bollani S, Bianchi Porro G (1996) Ultrasonographic detection of intestinal complications in Crohn’s disease. Dig Dis Sci 41:1643–1648
Gasche C, Moser G, Turetschek K et al (1999) Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut 44:112–117
Maconi G, Carsana L, Fociani P et al (2003) Small bowel stenosis in Crohn’s disease: clinical, biochemical and ultrasonographic evaluation of histological features. Aliment Pharmacol Ther 18:749–756
Andreoli A, Cerro P, Falasco G et al (1998) Role of ultrasonography in the diagnosis of postsurgical recurrence of Crohn’s disease. Am J Gastroenterol 93:1117–1121
Calabrese E, Petruzziello C, Onali S et al (2009) Severity of postoperative recurrence in Crohn’s disease: correlation between endoscopic and sonographic findings. Inflamm Bowel Dis 15:1635–1642
Nylund K, Hausken T, Gilja OH (2010) Ultrasound and inflammatory bowel disease. Ultrasound Q 26:3–15
Migaleddu V, Scanu AM, Quaia E et al (2009) Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn’s disease. Gastroenterology 137:43–52
Ripollés T, Martínez MJ, Paredes JM et al (2009) Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology 253:241–248
Calabrese E, La Seta F, Buccellato A et al (2005) Crohn’s disease: a comparative prospective study of transabdominal ultrasonography, small intestine contrast ultrasonography, and small bowel enema. Inflamm Bowel Dis 11:139–145
Pallotta N, Vincoli G, Montesani C et al (2012) Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in Crohn’s disease: a prospective comparative study versus intraoperative findings. Inflamm Bowel Dis 18:74–84
Pallotta N, Tomei E, Viscido A et al (2005) Small intestine contrast ultrasonography: an alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis 11:146–153
Calabrese E, Petruzziello C, Onali S et al (2009) Severity of postoperative recurrence in Crohn’s disease: correlation between endoscopic and sonographic findings. Inflamm Bowel Dis 15:1635–1642
Parente F, Greco S, Molteni M et al (2004) 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 53:1652–1657
Calabrese E, Zorzi F, Pallone F (2012) Ultrasound in Crohn’s disease. Curr Drug Targets 13:1224–1233
Pallotta N, Baccini F, Corazziari E (2001) Small intestine contrast ultrasonography (SICUS) in the diagnosis of small intestine lesions. Ultrasound Med Biol 27:335–341
Pallotta N, Civitelli F, Di Nardo G et al (2013) Small intestine contrast ultrasonography in pediatric Crohn’s disease. J Pediatr 163:778–784
Farmer RG, Whelan G, Fazio VW (1985) Long-term follow-up of patients with Crohn’s disease. Relationship between the clinical pattern and prognosis. Gastroenterology 88:1818–1825
Calabrese E, Zorzi F, Zuzzi S et al (2012) Development of a numerical index quantitating small bowel damage as detected by ultrasonography in Crohn’s disease. J Crohns Colitis 6:852–860
Chatu S, Pilcher J, Saxena SK et al (2012) Diagnostic accuracy of small intestine ultrasonography using an oral contrast agent in Crohn’s disease: comparative study from the UK. Clin Radiol 67:553–559
Calabrese E, Zorzi F, Onali S et al (2013) Accuracy of small-intestine contrast ultrasonography, compared with computed tomography enteroclysis, in characterizing lesions in patients with Crohn’s disease. Clin Gastroenterol Hepatol 11:950–955
Aloi M, Di Nardo G, Romano G et al (2015) Magnetic resonance enterography, small-intestine contrast US, and capsule endoscopy to evaluate the small bowel in pediatric Crohn’s disease: a prospective, blinded, comparison study. Gastrointest Endosc 81:420–427
Kumar S, Hakim A, Alexakis C et al (2015) 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 30:86–91
Futagami Y, Haruma K, Hata J et al (1999) Development and validation of an ultrasonographic activity index of Crohn’s disease. Eur J Gastroenterol Hepatol 11:1007–1012
Maconi G, Radice E, Greco S et al (2006) Bowel ultrasound in Crohn’s disease. Best Pract Res Clin Gastroenterol 20:93–112
Onali S, Calabrese E, Petruzziello C et al (2012) Small intestine contrast ultrasonography vs computed tomography enteroclysis for assessing ileal Crohn’s disease. World J Gastroenterol 18:6088–6095
Pallotta N, Giovannone M, Pezzotti P et al (2010) Ultrasonographic detection and assessment of the severity of Crohn’s disease recurrence after ileal resection. BMC Gastroenterol 10:69
Rutgeerts P, Geboes K, Vantrappen G et al (1984) Natural history of recurrent Crohn’s disease at the ileocolonic anastomosis after curative surgery. Gut 25:665–672
Castiglione F, Bucci L, Pesce G et al (2008) Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm Bowel Dis 14:1240–1245
Ribaldone DG, Cammarota T, Resegotti A et al (2014) Power doppler sonography to predict the risk of surgical recurrence of Crohn’s disease. J Ultrasound 18:51–55
Onali S, Calabrese E, Petruzziello C et al (2010) Endoscopic vs ultrasonographic findings related to Crohn’s disease recurrence: a prospective longitudinal study at 3 years. J Crohns Colitis 4:319–328
Rispo A, Bucci L, Pesce G et al (2006) Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm Bowel Dis 12:486–490
Frøslie KF, Jahnsen J, Moum BA et al (2007) IBSEN Group. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology 133:412–422
Solberg IC, Lygren I, Jahnsen J (2008) Mucosal healing after initial treatment may be a prognostic marker for long-term outcome in inflammatory bowel disease. Gut 57:A15
Baert F, Moortgat L, Van Assche G et al (2010) Belgian inflammatory bowel disease research group; North-Holland Gut Club. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn’s disease. Gastroenterology 138:463–468
Schnitzler F, Fidder H, Ferrante M et al (2009) Mucosal healing predicts long-term outcome of maintenance therapy with infliximab in Crohn’s disease. Inflamm Bowel Dis 15:1295–1301
Bruining DH, Loftus EV Jr, Ehman EC et al (2011) Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with Crohn’s disease. Clin Gastroenterol Hepatol 9:679–683
Van Assche G, Herrmann KA, Louis E et al (2013) Effects of infliximab therapy on transmural lesions as assessed by magnetic resonance enteroclysis in patients with ileal Crohn’s disease. J Crohns Colitis 7:950–957
Castiglione F, Testa A, Rea M et al (2013) Transmural healing evaluated by bowel sonography in patients with Crohn’s disease on maintenance treatment with biologics. Inflamm Bowel Dis 19:1928–1934
Ordás I, Rimola J, Rodríguez S et al (2014) Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn’s disease. Gastroenterology 146:374–382
Zorzi F, Stasi E, Bevivino G et al (2014) A sonographic lesion index for Crohn’s disease helps monitor changes in transmural bowel damage during therapy. Clin Gastroenterol Hepatol 12:2071–2077
Quaia E (2007) Contrast-specific ultrasound techniques. Radiol Med 112:473–490
Wilson SR, Burns PN (2010) Microbubble-enhanced US in body imaging: what role? Radiology 257:24–39
Piscaglia F, Bolondi L (2006) Italian society for ultrasound in medicine and biology (SIUMB) study group on ultrasound contrast agents. The safety of Sonovue in abdominal applications: retrospective analysis of 23188 investigations. Ultrasound Med Biol 32:1369–1375
Geleijnse ML, Nemes A, Vletter WB et al (2009) Adverse reactions after the use of sulphur hexafluoride (SonoVue) echo contrast agent. J Cardiovasc Med 10:75–77
Ma X, Li Y, Jia H et al (2015) Contrast-enhanced ultrasound in the diagnosis of patients suspected of having active Crohn’s disease: meta-analysis. Ultrasound Med Biol 41:659–668
Robotti D, Cammarota T, Debani P et al (2004) Activity of Crohn disease: value of color-power-doppler and contrast-enhanced ultrasonography. Abdom Imaging 29:648–652
Serra C, Menozzi G, Labate AM et al (2007) Ultrasound assessment of vascularization of the thickened terminal ileum wall in Crohn’s disease patients using a low-mechanical index real-time scanning technique with a second generation ultrasound contrast agent. Eur J Radiol 62:114–121
Parente F, Maconi G, Bollani S et al (2002) Bowel ultrasound in assessment of Crohn’s disease and detection of related small bowel strictures: a prospective comparative study versus x ray and intraoperative findings. Gut 50:490–495
Girlich C, Jung EM, Iesalnieks I et al (2009) Quantitative assessment of bowel wall vascularisation in Crohn’s disease with contrast-enhanced ultrasound and perfusion analysis. Clin Hemorheol Microcirc 43:141–148
Girlich C, Jung EM, Huber E et al (2011) Comparison between preoperative quantitative assessment of bowel wall vascularization by contrast-enhanced ultrasound and operative macroscopic findings and results of histopathological scoring in Crohn’s disease. Ultraschall Med 32:154–159
Girlich C, Schacherer D, Jung EM et al (2012) Comparison between a clinical activity index (harvey-bradshaw-index), laboratory inflammation markers and quantitative assessment of bowel wall vascularization by contrast-enhanced ultrasound in Crohn’s disease. Eur J Radiol 81:1105–1109
Ripollés T, Rausell N, Paredes JM et al (2013) Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn’s disease: a comparison with surgical histopathology analysis. J Crohns Colitis 7:120–128
Nylund K, Jirik R, Mezl M et al (2013) Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn’s disease. Ultrasound Med Biol 39:1197–1206
Quaia E, De Paoli L, Stocca T et al (2012) The value of small bowel wall contrast enhancement after sulfur hexafluoride-filled microbubble injection to differentiate inflammatory from fibrotic strictures in patients with Crohn’s disease. Ultrasound Med Biol 38:1324–1332
Ripollés T, Martínez MJ, Paredes JM et al (2009) Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology 253:241–248
Moreno N, Ripollés T, Paredes JM et al (2014) 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 Crohns Colitis 8:1079–1087
Quaia E, Migaleddu V, Baratella E et al (2009) The diagnostic value of small bowel wall vascularity after sulfur hexafluoride-filled microbubble injection in patients with Crohn’s disease. Correlation with the therapeutic effectiveness of specific anti-inflammatory treatment. Eur J Radiol 69:438–444
Quaia E, Cabibbo B, De Paoli L et al (2013) The value of time-intensity curves obtained after microbubble contrast agent injection to discriminate responders from non-responders to anti-inflammatory medication among patients with Crohn’s disease. Eur Radiol 23:1650–1659
Paredes JM, Ripollés T, Cortés X et al (2013) Contrast-enhanced ultrasonography: usefulness in the assessment of postoperative recurrence of Crohn’s disease. J Crohns Colitis 7:192–201
De Franco A, Di Veronica A, Armuzzi A et al (2012) Ileal Crohn disease: mural microvascularity quantified with contrast-enhanced US correlates with disease activity. Radiology 262:680–688
Guidi L, De Franco A, De Vitis I (2006) Contrast-enhanced ultrasonography with SonoVue after infliximab therapy in Crohn’s disease. Eur Rev Med Pharmacol Sci 10:23–26
Quaia E, Sozzi M, Angileri R et al (2016) Time-intensity curves obtained after microbubble injection can be used to differentiate responders from nonresponders among patients with clnically active Crohn’s disease after 6 weeks of pharmacologic treatment. Radiology 18:152461
Medellin-Kowalewski A, Wilkens R, Wilson A et al (2016) Quantitative contrast-enhanced ultrasound parameters in Crohn’s disease: their role in disease activity determination with ultrasound. Am J Roentgenol 206:64–73
Baumgart DC, Müller HP, Grittner U et al (2015) US-based real-time elastography for the detection of fibrotic gut tissue in patients with stricturing Crohn disease. Radiology 275:889–899
Fraquelli M, Branchi F, Cribiù FM et al (2015) The role of ultrasound elasticity imaging in predicting ileal fibrosis in Crohn’s disease patients. Inflamm Bowel Dis 21:2605–2612
Giannetti A, Randisi P, Stumpo M et al (2014) Diagnosis of one small bowel tumor: the role of conventional ultrasound and elastography. J Ultrasound 19:57–60
Giannetti A, Biscontri M, Matergi M et al (2016) Feasibility of CEUS and strain elastography in one case of ileum Crohn stricture and literature review. J Ultrasound 19:231–237
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This review was not funded by any grants.
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Mocci, G., Migaleddu, V., Cabras, F. et al. SICUS and CEUS imaging in Crohn’s disease: an update. J Ultrasound 20, 1–9 (2017). https://doi.org/10.1007/s40477-016-0230-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40477-016-0230-5