Skip to main content
Erschienen in: Pediatric Radiology 3/2021

07.01.2021 | Original Article

Contrast-enhanced ultrasonography in the evaluation of Crohn disease activity in children: comparison with histopathology

verfasst von: Slavojka Ponorac, Raja Dahmane Gošnak, Darja Urlep, Damjana Ključevšek

Erschienen in: Pediatric Radiology | Ausgabe 3/2021

Einloggen, um Zugang zu erhalten

Abstract

Background

Contrast-enhanced ultrasound (US) of the bowel wall has been suggested as an alternative imaging modality for the follow-up of children with Crohn disease.

Objective

To evaluate the diagnostic performance of contrast-enhanced US in the estimation of Crohn disease activity in children with histopathology as the reference standard.

Materials and methods

In 24 children with Crohn disease confirmed on histopathology, disease activity was evaluated on 40 bowel segments using US score and subjective and quantitative contrast-enhanced US evaluation. Contrast-enhanced US evaluation included enhancement pattern analysis with a graphic representation of log time-intensity curve and calculation of kinetic parameters with the definition of thresholds for disease activity, as determined by receiver operating characteristics curve analysis. The diagnostic accuracy of US with colour Doppler imaging and subjective and quantitative contrast-enhanced US were calculated.

Results

Moderate or severe inflammation was identified in 18 segments and remission or mild inflammation was identified in 22 segments on histopathology. The quantitative contrast-enhanced US, namely the peak enhancement value, had 72.2% sensitivity (95% confidence interval [CI] 46.5–90.3), 100% specificity (95% CI 84.6–100.0) and 87.5% diagnostic accuracy (95% CI 73.2–95.8) in predicting moderate or severe grade inflammation at histopathology. The sensitivity, specificity and diagnostic accuracy of subjective contrast-enhanced US were 77.8% (95% CI 52.4–93.6), 77.3% (95% CI 54.6–92.2) and 77.5% (95% CI 61.6–89.2), respectively, and of US with colour Doppler imaging were 55.6% (95% CI 30.8–78.5), 86.4% (95% CI 65.1–79.1) and 72.5% (95% CI 56.1–85.4), respectively.

Conclusion

Quantitative contrast-enhanced US has the potential of becoming a complementary method in the evaluation of Crohn disease activity in children. Fibrosis may affect peak enhancement results and underestimate inflammatory activity.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Schreiber-Dietrich D, Chiorean L, Cui XW et al (2015) Particularities of Crohn's disease in pediatric patients: current status and perspectives regarding imaging modalities. Expert Rev Gastroenterol Hepatol 9:1313–1325CrossRef Schreiber-Dietrich D, Chiorean L, Cui XW et al (2015) Particularities of Crohn's disease in pediatric patients: current status and perspectives regarding imaging modalities. Expert Rev Gastroenterol Hepatol 9:1313–1325CrossRef
2.
Zurück zum Zitat Esteban JM, Maldonado L, Sanchiz V et al (2001) Activity of Crohn's disease assessed by colour Doppler ultrasound analysis of the affected loops. Eur Radiol 11:1423–1428CrossRef Esteban JM, Maldonado L, Sanchiz V et al (2001) Activity of Crohn's disease assessed by colour Doppler ultrasound analysis of the affected loops. Eur Radiol 11:1423–1428CrossRef
3.
Zurück zum Zitat Horsthuis K, Bipat S, Bennink RJ, Stoker J (2008) Inflammatory bowel disease diagnosed with the US, MR, scintigraphy, and CT: a meta-analysis of prospective studies. Radiology 247:64–79CrossRef Horsthuis K, Bipat S, Bennink RJ, Stoker J (2008) Inflammatory bowel disease diagnosed with the US, MR, scintigraphy, and CT: a meta-analysis of prospective studies. Radiology 247:64–79CrossRef
4.
Zurück zum Zitat Sauer CG, Middleton JP, Alazraki A et al (2012) Comparison of magnetic resonance enterography with endoscopy, histopathology, and laboratory evaluation in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 55:178–184 Sauer CG, Middleton JP, Alazraki A et al (2012) Comparison of magnetic resonance enterography with endoscopy, histopathology, and laboratory evaluation in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 55:178–184
5.
Zurück zum Zitat Ripollés T, Martínez-Pérez MJ, Blanc E et al (2011) Contrast-enhanced ultrasound (CEUS) in Crohn's disease: technique, image interpretation, and clinical applications. Insights Imaging 2:639–652CrossRef Ripollés T, Martínez-Pérez MJ, Blanc E et al (2011) Contrast-enhanced ultrasound (CEUS) in Crohn's disease: technique, image interpretation, and clinical applications. Insights Imaging 2:639–652CrossRef
6.
Zurück zum Zitat Migaleddu V, Scanu AM, Quaia E et al (2009) Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn's disease. Gastroenterology 137:43–52CrossRef Migaleddu V, Scanu AM, Quaia E et al (2009) Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn's disease. Gastroenterology 137:43–52CrossRef
7.
Zurück zum Zitat Sidhu PS, Cantisani V, Deganello A et al (2017) Role of Contrast-Enhanced Ultrasound (CEUS) in Paediatric Practice: An EFSUMB Position Statement. Ultraschall Med 38:33–43PubMed Sidhu PS, Cantisani V, Deganello A et al (2017) Role of Contrast-Enhanced Ultrasound (CEUS) in Paediatric Practice: An EFSUMB Position Statement. Ultraschall Med 38:33–43PubMed
8.
Zurück zum Zitat Kljucevsek D, Vidmar D, Urlep D, Dežman R (2016) Dynamic contrast-enhanced ultrasound of the bowel wall with quantitative assessment of Crohn's disease activity in childhood. Radiol Oncol 50:347–354CrossRef Kljucevsek D, Vidmar D, Urlep D, Dežman R (2016) Dynamic contrast-enhanced ultrasound of the bowel wall with quantitative assessment of Crohn's disease activity in childhood. Radiol Oncol 50:347–354CrossRef
9.
Zurück zum Zitat Tang MX, Mulvana H, Gauthier T et al (2011) Quantitative contrast-enhanced ultrasound imaging: A review of sources of variability. Interface Focus 1:520–539CrossRef Tang MX, Mulvana H, Gauthier T et al (2011) Quantitative contrast-enhanced ultrasound imaging: A review of sources of variability. Interface Focus 1:520–539CrossRef
10.
Zurück zum Zitat Biko DM, Rosenbaum DG, Anupindi SA (2015) Ultrasound features of pediatric Crohn disease: a guide for case interpretation. Pediatr Radiol 45:1557–1566CrossRef Biko DM, Rosenbaum DG, Anupindi SA (2015) Ultrasound features of pediatric Crohn disease: a guide for case interpretation. Pediatr Radiol 45:1557–1566CrossRef
11.
Zurück zum Zitat 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 206:64–73CrossRef 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 206:64–73CrossRef
12.
Zurück zum Zitat Akhbardeh A, Sagreiya H, Kaffas AE et al (2019) A Multi-Model Framework to Estimate Perfusion Parameters Using Contrast-Enhanced Ultrasound Imaging. Med Phys 46:590–600CrossRef Akhbardeh A, Sagreiya H, Kaffas AE et al (2019) A Multi-Model Framework to Estimate Perfusion Parameters Using Contrast-Enhanced Ultrasound Imaging. Med Phys 46:590–600CrossRef
13.
Zurück zum Zitat Dietrich CF, Averkiou MA, Correas JM et al (2012) An EFSUMB Introduction into dynamic contrast-enhanced ultrasound (DCE-US) for quantification of tumor-perfusion. Ultraschall Med 33:344–351CrossRef Dietrich CF, Averkiou MA, Correas JM et al (2012) An EFSUMB Introduction into dynamic contrast-enhanced ultrasound (DCE-US) for quantification of tumor-perfusion. Ultraschall Med 33:344–351CrossRef
14.
Zurück zum Zitat Medellin A, Merrill C, Wilson SR (2018) Role of contrast-enhanced ultrasound in the evaluation of the bowel. Abdom Radiol (NY) 43:918–933CrossRef Medellin A, Merrill C, Wilson SR (2018) Role of contrast-enhanced ultrasound in the evaluation of the bowel. Abdom Radiol (NY) 43:918–933CrossRef
15.
Zurück zum Zitat Agrawal M, Colombel JF (2019) Treat-to-Target in Inflammatory Bowel Diseases, What Is the Target and How Do We Treat? Gastrointest Endosc Clin N Am 29:421–436CrossRef Agrawal M, Colombel JF (2019) Treat-to-Target in Inflammatory Bowel Diseases, What Is the Target and How Do We Treat? Gastrointest Endosc Clin N Am 29:421–436CrossRef
16.
Zurück zum Zitat Gong W, Guo K, Zheng T et al (2019) Correlation between endoscopic and histological validated scoring indices in Crohn's disease. Dig Liver Dis 51:812–817 Gong W, Guo K, Zheng T et al (2019) Correlation between endoscopic and histological validated scoring indices in Crohn's disease. Dig Liver Dis 51:812–817
17.
Zurück zum Zitat Romanini L, Passamonti M, Navarria M et al (2014) Quantitative analysis of contrast-enhanced ultrasonography of the bowel wall can predict disease activity in inflammatory bowel disease. Eur J Radiol 83:1317–1323CrossRef Romanini L, Passamonti M, Navarria M et al (2014) Quantitative analysis of contrast-enhanced ultrasonography of the bowel wall can predict disease activity in inflammatory bowel disease. Eur J Radiol 83:1317–1323CrossRef
18.
Zurück zum Zitat Ripolle's 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 7:120–128CrossRef Ripolle's 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 7:120–128CrossRef
19.
Zurück zum Zitat Quaia E, De Paoli L, Stock 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 38:1324–1332CrossRef Quaia E, De Paoli L, Stock 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 38:1324–1332CrossRef
20.
Zurück zum Zitat 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 39:1197–1206CrossRef 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 39:1197–1206CrossRef
21.
Zurück zum Zitat Wilkens R, Hagemann-Madsen RH, Peters DA et al (2018) Validity of contrast-enhanced ultrasonography and dynamic contrast-enhanced MR enterography in the assessment of transmural activity and fibrosis in Crohn's disease. J Crohns Colitis 12:48–56CrossRef Wilkens R, Hagemann-Madsen RH, Peters DA et al (2018) Validity of contrast-enhanced ultrasonography and dynamic contrast-enhanced MR enterography in the assessment of transmural activity and fibrosis in Crohn's disease. J Crohns Colitis 12:48–56CrossRef
22.
Zurück zum Zitat Dillman JR, Rubin JM, Johanson LA et al (2017) Can contrast-enhanced sonography detect bowel wall fibrosis in mixed inflammatory and fibrotic Crohn disease lesions in an animal model? J Ultrasound Med 36:523–530CrossRef Dillman JR, Rubin JM, Johanson LA et al (2017) Can contrast-enhanced sonography detect bowel wall fibrosis in mixed inflammatory and fibrotic Crohn disease lesions in an animal model? J Ultrasound Med 36:523–530CrossRef
23.
Zurück zum Zitat Thimm MA, Cuffari C, Garcia A et al (2019) Contrast-Enhanced Ultrasound and Shear Wave Elastography Evaluation of Crohn's disease Activity in Three Adolescent Patients. Pediatr Gastroenterol Hepatol Nutr 22:282–290CrossRef Thimm MA, Cuffari C, Garcia A et al (2019) Contrast-Enhanced Ultrasound and Shear Wave Elastography Evaluation of Crohn's disease Activity in Three Adolescent Patients. Pediatr Gastroenterol Hepatol Nutr 22:282–290CrossRef
24.
Zurück zum Zitat Quaia E, Gennari AG, Cova MA, van Beek EJ (2018) Differentiation of inflammatory from fibrotic ileal strictures among patients with Crohn's disease based on visual analysis: feasibility study combining conventional B-mode ultrasound, contrast-enhanced ultrasound and strain elastography. Ultrasound Med Biol 44:762–770CrossRef Quaia E, Gennari AG, Cova MA, van Beek EJ (2018) Differentiation of inflammatory from fibrotic ileal strictures among patients with Crohn's disease based on visual analysis: feasibility study combining conventional B-mode ultrasound, contrast-enhanced ultrasound and strain elastography. Ultrasound Med Biol 44:762–770CrossRef
25.
Zurück zum Zitat 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 vascularisation by contrast-enhanced ultrasound in Crohn's disease. Eur J Radiol 81:1105–1109CrossRef 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 vascularisation by contrast-enhanced ultrasound in Crohn's disease. Eur J Radiol 81:1105–1109CrossRef
26.
Zurück zum Zitat De Franco A, Di Veronica A, Armuzzi A et al (2012) Ileal Crohn disease: mural microvascularity quantified with the contrast-enhanced US correlates with disease activity. Radiology 262:680–688CrossRef De Franco A, Di Veronica A, Armuzzi A et al (2012) Ileal Crohn disease: mural microvascularity quantified with the contrast-enhanced US correlates with disease activity. Radiology 262:680–688CrossRef
27.
Zurück zum Zitat 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 69:438–444CrossRef 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 69:438–444CrossRef
28.
Zurück zum Zitat 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 Clinically Active Crohn Disease after 6 Weeks of Pharmacologic Treatment. Radiology 281:606–616CrossRef 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 Clinically Active Crohn Disease after 6 Weeks of Pharmacologic Treatment. Radiology 281:606–616CrossRef
29.
Zurück zum Zitat Saevik F, Nylund K, Hausken T et al (2014) Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn's disease. Inflamm Bowel Dis 20:2029–2037CrossRef Saevik F, Nylund K, Hausken T et al (2014) Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn's disease. Inflamm Bowel Dis 20:2029–2037CrossRef
30.
Zurück zum Zitat Ntoulia A, Anupindi SA, Darge K, Back SJ (2018) Applications of contrast-enhanced ultrasound in the pediatric abdomen. Abdom Radiol (NY) 43:948–959CrossRef Ntoulia A, Anupindi SA, Darge K, Back SJ (2018) Applications of contrast-enhanced ultrasound in the pediatric abdomen. Abdom Radiol (NY) 43:948–959CrossRef
31.
Zurück zum Zitat Piskunowicz M, Kosiak W, Batko T et al (2015) Safety of intravenous application of second-generation ultrasound contrast agent in children: a prospective analysis. Ultrasound Med Biol 41:1095–1099CrossRef Piskunowicz M, Kosiak W, Batko T et al (2015) Safety of intravenous application of second-generation ultrasound contrast agent in children: a prospective analysis. Ultrasound Med Biol 41:1095–1099CrossRef
32.
Zurück zum Zitat Knieling F, Strobel D, Rompel O et al (2016) Spectrum, applicability and diagnostic capacity of contrast-enhanced ultrasound in pediatric patients and young adults after intravenous application—a retrospective trial. Ultraschall Med 37:619–626CrossRef Knieling F, Strobel D, Rompel O et al (2016) Spectrum, applicability and diagnostic capacity of contrast-enhanced ultrasound in pediatric patients and young adults after intravenous application—a retrospective trial. Ultraschall Med 37:619–626CrossRef
33.
Zurück zum Zitat Coudray S, Fabre C, Aichoun I, Perez-Martin A (2017) Anaphylactic shock with an ultrasound contrast agent. J Med Vasc 42:384–387PubMed Coudray S, Fabre C, Aichoun I, Perez-Martin A (2017) Anaphylactic shock with an ultrasound contrast agent. J Med Vasc 42:384–387PubMed
34.
Zurück zum Zitat Sidhu PS, Cantisani V, Dietrich CF et al (2018) The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Long Version). Ultraschall Med 39:e2–e44CrossRef Sidhu PS, Cantisani V, Dietrich CF et al (2018) The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Long Version). Ultraschall Med 39:e2–e44CrossRef
Metadaten
Titel
Contrast-enhanced ultrasonography in the evaluation of Crohn disease activity in children: comparison with histopathology
verfasst von
Slavojka Ponorac
Raja Dahmane Gošnak
Darja Urlep
Damjana Ključevšek
Publikationsdatum
07.01.2021
Verlag
Springer Berlin Heidelberg
Erschienen in
Pediatric Radiology / Ausgabe 3/2021
Print ISSN: 0301-0449
Elektronische ISSN: 1432-1998
DOI
https://doi.org/10.1007/s00247-020-04870-3

Weitere Artikel der Ausgabe 3/2021

Pediatric Radiology 3/2021 Zur Ausgabe

Hermes

Hermes

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.