Intestinal Ultrasound and its Application as Point-of-Care Procedure for Diagnosing and Detecting Inflammatory Bowel Disease and Related Complications: A Narrative Review
Main Article Content
Abstract
Inflammatory bowel disease, comprising Crohn's disease and ulcerative colitis, defines as an idiopathic, chronic, relapsing, inflammatory disease affecting the gastrointestinal tract and leading to chronic damage. Endoscopy with biopsies is considered the gold standard for inflammatory bowel disease diagnosis, whereas magnetic resonance for Crohn’s disease extension and complication assessment. However, colonoscopy is an invasive procedure, while magnetic resonance is relatively not easily accessible for patients; thus, the need for a reliable, accessible and non-invasive way to perform inflammatory bowel diseases diagnosis and monitoring in the tight control era, like intestinal ultrasound is. Compared to endoscopy and magnetic resonance, ultrasound has shown reliable diagnostic accuracy in assessing Crohn’s disease diagnosis and evaluation of localisation, extension and complications. On the other hand, intestinal ultrasound is emerging as a valid tool also for ulcerative colitis severity and extension assessment. Moreover, performing ultrasonography in a point-of-care setting can guide the clinician in driving the diagnostic and therapeutic pathway, thus accelerating clinical decisions. As a novelty, point-of-care intestinal ultrasound performed with pocket devices could represent a promising item for the future of physical examination in outpatient or inpatient examination. The need for reproducibility of intestinal ultrasound among sonographers has emerged as a key-point in inflammatory bowel disease research field: the development of new scores for the evaluation of disease severity together with an intensive dedicated trainship could potentially reduce the differences between clinicians reporting.
Accordingly, our aim was to perform a narrative review about the application of intestinal ultrasound in Crohn’s disease and ulcerative colitis diagnosis and monitoring. Furthermore, technical aspects of this imaging technique and its application in a point-of-care setting through traditional and handheld sonographers were explored.
Keywords:
IBD, Crohn, Ulcerative colitis, diagnosis, intestinal ultrasonography, POCIUS
Article Details
How to Cite
RISPO, Antonio et al.
Intestinal Ultrasound and its Application as Point-of-Care Procedure for Diagnosing and Detecting Inflammatory Bowel Disease and Related Complications: A Narrative Review.
Medical Research Archives, [S.l.], v. 11, n. 10, oct. 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4472>. Date accessed: 15 may 2024.
doi: https://doi.org/10.18103/mra.v11i10.4472.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Kaplan GG, Windsor JW. The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2021;18(1):56-66. doi:10.1038/s41575-020-00360-x
2. Turner D, Ricciuto A, Lewis A, 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(5):1570-1583. doi:10.1053/j.gastro.2020.12.031
3. Maaser C, Sturm A, Vavricka SR, et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. Journal of Crohn’s and Colitis. 2019;13(2):144-164K. doi:10.1093/ecco-jcc/jjy113
4. Magro F, Gionchetti P, Eliakim R, et al. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 1: Definitions, Diagnosis, Extra-intestinal Manifestations, Pregnancy, Cancer Surveillance, Surgery, and Ileo-anal Pouch Disorders. Journal of Crohn’s and Colitis. 2017;11(6):649-670. doi:10.1093/ecco-jcc/jjx008
5. Rimola J, Torres J, Kumar S, Taylor SA, Kucharzik T. Recent advances in clinical practice: advances in cross-sectional imaging in inflammatory bowel disease. Gut. Published online August 4, 2022:gutjnl-2021-326562. doi:10.1136/gutjnl-2021-326562
6. Bots S, De Voogd F, De Jong M, et al. 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. Journal of Crohn’s and Colitis. 2022;16(4):606-615. doi:10.1093/ecco-jcc/jjab175
7. de Voogd FAE, Verstockt B, Maaser C, Gecse KB. Point-of-care intestinal ultrasonography in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2021;18(4):209-210. doi:10.1038/s41575-021-00418-4
8. Nardone OM, Calabrese G, Testa A, et al. The Impact of Intestinal Ultrasound on the Management of Inflammatory Bowel Disease: From Established Facts Toward New Horizons. Front Med. 2022;9:898092. doi:10.3389/fmed.2022.898092
9. Allocca M, Furfaro F, Fiorino G, Peyrin-Biroulet L, Danese S. Point-of-Care Ultrasound in Inflammatory Bowel Disease. Journal of Crohn’s and Colitis. 2021;15(1):143-151. doi:10.1093/ecco-jcc/jjaa151
10. Allocca M, Kucharzik T, Rubin DT. Intestinal Ultrasound in the Assessment and Management of Inflammatory Bowel Disease: Is It Ready for Standard Practice? Gastroenterology. 2023;164(6):851-855. doi:10.1053/j.gastro.2023.01.021
11. Kucharzik T, Tielbeek J, Carter D, et al. ECCO-ESGAR Topical Review on Optimizing Reporting for Cross-Sectional Imaging in Inflammatory Bowel Disease. Journal of Crohn’s and Colitis. 2022;16(4):523-543. doi:10.1093/ecco-jcc/jjab180
12. Maconi G, Parente F, Bollani S, Cesana B, Bianchi Porro G. Abdominal ultrasound in the assessment of extent and activity of Crohn’s disease: clinical significance and implication of bowel wall thickening. Am J Gastroenterol. 1996;91(8):1604-1609.
13. Astegiano M, Bresso F, Cammarota T, et al. Abdominal pain and bowel dysfunction: diagnostic role of intestinal ultrasound: European Journal of Gastroenterology & Hepatology. 2001;13(8):927-931. doi:10.1097/00042737-200108000-00009
14. Parente F. 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. 2002;50(4):490-495. doi:10.1136/gut.50.4.490
15. Pascu M, Roznowski AB, Müller HP, Adler A, Wiedenmann B, Dignass AU. Clinical Relevance of Transabdominal Ultrasonography and Magnetic Resonance Imaging in Patients With Inflammatory Bowel Disease of the Terminal Ileum and Large Bowel: Inflammatory Bowel Diseases. 2004;10(4):373-382. doi:10.1097/00054725-200407000-00008
16. Pallotta N, Tomei E, Viscido A, et al. Small Intestine Contrast Ultrasonography: An Alternative to Radiology in the Assessment of Small Bowel Disease. Inflammatory Bowel Diseases. 2005;11(2):146-153. doi:10.1097/00054725-200502000-00008
17. Rispo A, Imbriaco M, Celentano L, et al. Noninvasive Diagnosis of Small Bowel Crohnʼs Disease: Combined Use of Bowel Sonography and Tc-99M-Hmpao Leukocyte Scintigraphy: Inflammatory Bowel Diseases. 2005;11(4):376-382. doi:10.1097/01.MIB.0000164020.65106.84
18. Castiglione F, Mainenti PP, De Palma GD, et al. Noninvasive Diagnosis of Small Bowel Crohn’s Disease: Direct Comparison of Bowel Sonography and Magnetic Resonance Enterography. Inflammatory Bowel Diseases. 2013;19(5):991-998. doi:10.1097/MIB.0b013e3182802b87
19. Pallotta N, Civitelli F, Di Nardo G, et al. Small Intestine Contrast Ultrasonography in Pediatric Crohn’s Disease. The Journal of Pediatrics. 2013;163(3):778-784.e1. doi:10.1016/j.jpeds.2013.03.056
20. Rispo A, de Sire R, Mainenti PP, et al. David Against Goliath: Direct Comparison of Handheld Bowel Sonography and Magnetic Resonance Enterography for Diagnosis of Crohn’s Disease. Inflammatory Bowel Diseases. Published online June 6, 2022:izac116. doi:10.1093/ibd/izac116
21. Calabrese E, Maaser C, Zorzi F, et al. Bowel Ultrasonography in the Management of Crohnʼs Disease. A Review with Recommendations of an International Panel of Experts: Inflammatory Bowel Diseases. 2016;22(5):1168-1183. doi:10.1097/MIB.0000000000000706
22. Taylor SA, Mallett S, Bhatnagar G, 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. The Lancet Gastroenterology & Hepatology. 2018;3(8):548-558. doi:10.1016/S2468-1253(18)30161-4
23. Reimund JM, Jung-Chaigneau E, Chamouard P, Wittersheim C, Duclos B, Baumann R. [Diagnostic value of high resolution sonography in Crohn’s disease and ulcerative colitis]. Gastroenterol Clin Biol. 1999;23(6-7):740-746.
24. Bru C, Sans M, Defelitto MM, et al. Hydrocolonic Sonography for Evaluating Inflammatory Bowel Disease. American Journal of Roentgenology. 2001;177(1):99-105. doi:10.2214/ajr.177.1.1770099
25. Parente F, Greco S, Molteni M, et al. Role of early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel: BOWEL ULTRASOUND FOR DETECTION OF INFLAMMATORY DISEASE. Alimentary Pharmacology & Therapeutics. 2003;18(10):1009-1016. doi:10.1046/j.1365-2036.2003.01796.x
26. Parente F. 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(11):1652-1657. doi:10.1136/gut.2004.041038
27. Martínez MJ, Ripollés T, Paredes JM, Blanc E, Martí-Bonmatí L. Assessment of the extension and the inflammatory activity in Crohn’s disease: comparison of ultrasound and MRI. Abdom Imaging. 2009;34(2):141-148. doi:10.1007/s00261-008-9365-y
28. Rispo A, Imperatore N, Testa A, et al. Bowel Damage in Crohnʼs Disease: Direct Comparison of Ultrasonography-based and Magnetic Resonance-based Lemann Index. Inflammatory Bowel Diseases. 2017;23(1):143-151. doi:10.1097/MIB.0000000000000980
29. Allocca M, Fiorino G, Bonifacio C, et al. Comparative Accuracy of Bowel Ultrasound Versus Magnetic Resonance Enterography in Combination With Colonoscopy in Assessing Crohn’s Disease and Guiding Clinical Decision-making. Journal of Crohn’s and Colitis. 2018;12(11):1280-1287. doi:10.1093/ecco-jcc/jjy093
30. Panés J, Bouzas R, Chaparro M, 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: Systematic review: cross-sectional imaging in Crohn’s disease. Alimentary Pharmacology & Therapeutics. 2011;34(2):125-145. doi:10.1111/j.1365-2036.2011.04710.x
31. Calabrese E, La Seta F, Buccellato A, et al. Crohnʼs Disease: A Comparative Prospective Study of Transabdominal Ultrasonography, Small Intestine Contrast Ultrasonography, and Small Bowel Enema: Inflammatory Bowel Diseases. 2005;11(2):139-145. doi:10.1097/00054725-200502000-00007
32. Ismail MS, Charabaty A. Management of Crohn’s stricture: medical, endoscopic and surgical therapies. Frontline Gastroenterol. 2022;13(6):524-530. doi:10.1136/flgastro-2021-101827
33. Gasche C, Moser G, Turetschek K, Schober E, Moeschl P, Oberhuber G. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut. 1999;44(1):112-117. doi:10.1136/gut.44.1.112
34. Kohn A, Cerro P, Milite G, De Angelis E, Prantera C. Prospective Evaluation of Transabdominal Bowel Sonography in the Diagnosis of Intestinal Obstruction in Crohnʼs Disease: Comparison with Plain Abdominal Film and Small Bowel Enteroclysis: Inflammatory Bowel Diseases. 1999;5(3):153-157. doi:10.1097/00054725-199908000-00001
35. Pallotta N, Vincoli G, Montesani C, et al. Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in crohnʼs disease: A prospective comparative study versus intraoperative findings: Inflammatory Bowel Diseases. 2012;18(1):74-84. doi:10.1002/ibd.21678
36. Onali S. Small intestine contrast ultrasonography vs computed tomography enteroclysis for assessing ileal Crohn’s disease. WJG. 2012;18(42):6088. doi:10.3748/wjg.v18.i42.6088
37. Kumar S, Hakim A, Alexakis C, et al. Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn’s disease: Correlation with intraoperative findings and magnetic resonance enterography: Small intestinal contrast ultrasonography in Crohn’s disease. J Gastroenterol Hepatol. 2015;30(1):86-91. doi:10.1111/jgh.12724
38. Maconi G, Sampietro GM, Parente F, et al. Contrast Radiology, Computed Tomography and Ultrasonography in Detecting Internal Fistulas and Intra-Abdominal Abscesses in Crohn’s Disease: A Prospective Comparative Study. American Journal of Gastroenterology. 2003;98(7):1545-1555. doi:10.1111/j.1572-0241.2003.07521.x
39. Grażyńska A, Kufel J, Dudek A, Cebula M. Shear Wave and Strain Elastography in Crohn’s Disease—A Systematic Review. Diagnostics. 2021;11(9):1609. doi:10.3390/diagnostics11091609
40. Torres J, Mehandru S, Colombel JF, Peyrin-Biroulet L. Crohn’s disease. The Lancet. 2017;389(10080):1741-1755. doi:10.1016/S0140-6736(16)31711-1
41. Adamina M, Bonovas S, Raine T, et al. ECCO Guidelines on Therapeutics in Crohn’s Disease: Surgical Treatment. Journal of Crohn’s and Colitis. 2020;14(2):155-168. doi:10.1093/ecco-jcc/jjz187
42. Rispo A, Imperatore N, Testa A, et al. Diagnostic Accuracy of Ultrasonography in the Detection of Postsurgical Recurrence in Crohn’s Disease: A Systematic Review with Meta-analysis. Inflammatory Bowel Diseases. 2018;24(5):977-988. doi:10.1093/ibd/izy012
43. Andreoli A, Prantera C. Role of Ultrasonography in the Diagnosis of Postsurgical Recurrence of Crohn’s Disease. 1998;93(7).
44. Rispo A, Bucci L, Pesce G, et al. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohnʼs disease: Inflammatory Bowel Diseases. 2006;12(6):486-490. doi:10.1097/00054725-200606000-00007
45. Castiglione F, Bucci L, Pesce G, et al. Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohnʼs disease: Inflammatory Bowel Diseases. 2008;14(9):1240-1245. doi:10.1002/ibd.20469
46. Calabrese E, Petruzziello C, Onali S, et al. Severity of postoperative recurrence in crohnʼs disease: Correlation between endoscopic and sonographic findings: Inflammatory Bowel Diseases. 2009;15(11):1635-1642. doi:10.1002/ibd.20948
47. Onali S, Calabrese E, Petruzziello C, et al. Post-operative recurrence of Crohn’s disease: A prospective study at 5 years. Digestive and Liver Disease. 2016;48(5):489-494. doi:10.1016/j.dld.2016.01.009
48. Dal Piaz G, Mendolaro M, Mineccia M, et al. Predictivity of early and late assessment for post-surgical recurrence of Crohn’s disease: Data from a single-center retrospective series. Digestive and Liver Disease. 2021;53(8):987-995. doi:10.1016/j.dld.2020.09.018
49. S. Hollerbach, A. Geissler, H. Schi. The Accuracy of Abdominal Ultrasound in the Assessment of Bowel Disorders. Scandinavian Journal of Gastroenterology. 1998;33(11):1201-1208. doi:10.1080/00365529850172575
50. Truong M, Atri M, Bret PM, et al. Sonographic appearance of benign and malignant conditions of the colon. American Journal of Roentgenology. 1998;170(6):1451-1455. doi:10.2214/ajr.170.6.9609152
51. Lim JH, Ko YT, Lee DH, Lim JW, Kim TH. Sonography of inflammatory bowel disease: findings and value in differential diagnosis. American Journal of Roentgenology. 1994;163(2):343-347. doi:10.2214/ajr.163.2.8037027
52. Schwerck W, Beckh K, Raith M. A prospective evaluation of high resolution sonography in the diagnosis of inflammatory bowel disease.
53. Allocca M, Fiorino G, Bonovas S, et al. Accuracy of Humanitas Ultrasound Criteria in Assessing Disease Activity and Severity in Ulcerative Colitis: A Prospective Study. Journal of Crohn’s and Colitis. 2018;12(12):1385-1391. doi:10.1093/ecco-jcc/jjy107
54. Kinoshita K, Katsurada T, Nishida M, et al. Usefulness of transabdominal ultrasonography for assessing ulcerative colitis: a prospective, multicenter study. J Gastroenterol. 2019;54(6):521-529. doi:10.1007/s00535-018-01534-w
55. Sagami S, Kobayashi T, Miyatani Y, et al. Accuracy of Ultrasound for Evaluation of Colorectal Segments in Patients With Inflammatory Bowel Diseases: A Systematic Review and Meta-analysis. Clinical Gastroenterology and Hepatology. 2021;19(5):908-921.e6. doi:10.1016/j.cgh.2020.07.067
56. Bozkurt T, Rommel T, Stabenow-Lohbauer U, Langer M, Schmiegelow P, Lux G. Sonographic bowel wall morphology correlates with clinical and endoscopic activity in crohn’s disease and ulcerative colitis. European Journal of Ultrasound. 1996;4(1):27-33. doi:10.1016/0929-8266(95)00169-7
57. Antonelli E, Giuliano V, Casella G, et al. Ultrasonographic assessment of colonic wall in moderate–severe ulcerative colitis: Comparison with endoscopic findings. Digestive and Liver Disease. 2011;43(9):703-706. doi:10.1016/j.dld.2011.02.019
58. Allocca M, Filippi E, Costantino A, et al. Milan ultrasound criteria are accurate in assessing disease activity in ulcerative colitis: external validation. United European Gastroenterol j. 2021;9(4):438-442. doi:10.1177/2050640620980203
59. Bots S, Nylund K, Löwenberg M, Gecse K, D’Haens G. Intestinal Ultrasound to Assess Disease Activity in Ulcerative Colitis: Development of a novel UC-Ultrasound Index. Journal of Crohn’s and Colitis. 2021;15(8):1264-1271. doi:10.1093/ecco-jcc/jjab002
60. Fraquelli M, Sarno A, Girelli C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn’s disease. Digestive and Liver Disease. 2008;40(11):860-866. doi:10.1016/j.dld.2008.04.006
61. De Voogd F, Wilkens R, Gecse K, et al. A Reliability Study: Strong Inter-Observer Agreement of an Expert Panel for Intestinal Ultrasound in Ulcerative Colitis. Journal of Crohn’s and Colitis. 2021;15(8):1284-1290. doi:10.1093/ecco-jcc/jjaa267
62. Novak KL, Nylund K, Maaser C, 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. Journal of Crohn’s and Colitis. 2021;15(4):609-616. doi:10.1093/ecco-jcc/jjaa216
63. Allocca M, Craviotto V, Dell’Avalle C, et al. Bowel ultrasound score is accurate in assessing response to therapy in patients with Crohn’s disease. Aliment Pharmacol Ther. 2022;55(4):446-454. doi:10.1111/apt.16700
64. Allocca M, Dell’Avalle C, Craviotto V, et al. Predictive value of Milan ultrasound criteria in ulcerative colitis: A prospective observational cohort study. UEG Journal. 2022;10(2):190-197. doi:10.1002/ueg2.12206
65. Mjolstad OC, Dalen H, Graven T, Kleinau JO, Salvesen O, Haugen BO. Routinely adding ultrasound examinations by pocket-sized ultrasound devices improves inpatient diagnostics in a medical department. European Journal of Internal Medicine. 2012;23(2):185-191. doi:10.1016/j.ejim.2011.10.009
66. Wastl D, Löwe A, Dietrich CF. Echoscopy in scanning abdominal diseases in a critical care setting. Med Klin Intensivmed Notfmed. Published online June 2, 2022. doi:10.1007/s00063-022-00926-4
67. Barreiros A, Cui X, Ignee A, De Molo C, Pirri C, Dietrich C. EchoScopy in Scanning Abdominal Diseases: Initial Clinical Experience. Z Gastroenterol. 2014;52(03):269-275. doi:10.1055/s-0033-1350114
68. Testuz A, Muller H, Keller PF, et al. Diagnostic accuracy of pocket-size handheld echocardiographs used by cardiologists in the acute care setting. European Heart Journal - Cardiovascular Imaging. 2013;14(1):38-42. doi:10.1093/ehjci/jes085
69. Rispo A, Calabrese G, Testa A, et al. Hocus Pocus: the Role of Hand-held Ultrasonography in Predicting Disease Extension and Endoscopic Activity in Ulcerative Colitis. Journal of Crohn’s and Colitis. Published online February 16, 2023:jjad024. doi:10.1093/ecco-jcc/jjad024
2. Turner D, Ricciuto A, Lewis A, 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(5):1570-1583. doi:10.1053/j.gastro.2020.12.031
3. Maaser C, Sturm A, Vavricka SR, et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. Journal of Crohn’s and Colitis. 2019;13(2):144-164K. doi:10.1093/ecco-jcc/jjy113
4. Magro F, Gionchetti P, Eliakim R, et al. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 1: Definitions, Diagnosis, Extra-intestinal Manifestations, Pregnancy, Cancer Surveillance, Surgery, and Ileo-anal Pouch Disorders. Journal of Crohn’s and Colitis. 2017;11(6):649-670. doi:10.1093/ecco-jcc/jjx008
5. Rimola J, Torres J, Kumar S, Taylor SA, Kucharzik T. Recent advances in clinical practice: advances in cross-sectional imaging in inflammatory bowel disease. Gut. Published online August 4, 2022:gutjnl-2021-326562. doi:10.1136/gutjnl-2021-326562
6. Bots S, De Voogd F, De Jong M, et al. 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. Journal of Crohn’s and Colitis. 2022;16(4):606-615. doi:10.1093/ecco-jcc/jjab175
7. de Voogd FAE, Verstockt B, Maaser C, Gecse KB. Point-of-care intestinal ultrasonography in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2021;18(4):209-210. doi:10.1038/s41575-021-00418-4
8. Nardone OM, Calabrese G, Testa A, et al. The Impact of Intestinal Ultrasound on the Management of Inflammatory Bowel Disease: From Established Facts Toward New Horizons. Front Med. 2022;9:898092. doi:10.3389/fmed.2022.898092
9. Allocca M, Furfaro F, Fiorino G, Peyrin-Biroulet L, Danese S. Point-of-Care Ultrasound in Inflammatory Bowel Disease. Journal of Crohn’s and Colitis. 2021;15(1):143-151. doi:10.1093/ecco-jcc/jjaa151
10. Allocca M, Kucharzik T, Rubin DT. Intestinal Ultrasound in the Assessment and Management of Inflammatory Bowel Disease: Is It Ready for Standard Practice? Gastroenterology. 2023;164(6):851-855. doi:10.1053/j.gastro.2023.01.021
11. Kucharzik T, Tielbeek J, Carter D, et al. ECCO-ESGAR Topical Review on Optimizing Reporting for Cross-Sectional Imaging in Inflammatory Bowel Disease. Journal of Crohn’s and Colitis. 2022;16(4):523-543. doi:10.1093/ecco-jcc/jjab180
12. Maconi G, Parente F, Bollani S, Cesana B, Bianchi Porro G. Abdominal ultrasound in the assessment of extent and activity of Crohn’s disease: clinical significance and implication of bowel wall thickening. Am J Gastroenterol. 1996;91(8):1604-1609.
13. Astegiano M, Bresso F, Cammarota T, et al. Abdominal pain and bowel dysfunction: diagnostic role of intestinal ultrasound: European Journal of Gastroenterology & Hepatology. 2001;13(8):927-931. doi:10.1097/00042737-200108000-00009
14. Parente F. 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. 2002;50(4):490-495. doi:10.1136/gut.50.4.490
15. Pascu M, Roznowski AB, Müller HP, Adler A, Wiedenmann B, Dignass AU. Clinical Relevance of Transabdominal Ultrasonography and Magnetic Resonance Imaging in Patients With Inflammatory Bowel Disease of the Terminal Ileum and Large Bowel: Inflammatory Bowel Diseases. 2004;10(4):373-382. doi:10.1097/00054725-200407000-00008
16. Pallotta N, Tomei E, Viscido A, et al. Small Intestine Contrast Ultrasonography: An Alternative to Radiology in the Assessment of Small Bowel Disease. Inflammatory Bowel Diseases. 2005;11(2):146-153. doi:10.1097/00054725-200502000-00008
17. Rispo A, Imbriaco M, Celentano L, et al. Noninvasive Diagnosis of Small Bowel Crohnʼs Disease: Combined Use of Bowel Sonography and Tc-99M-Hmpao Leukocyte Scintigraphy: Inflammatory Bowel Diseases. 2005;11(4):376-382. doi:10.1097/01.MIB.0000164020.65106.84
18. Castiglione F, Mainenti PP, De Palma GD, et al. Noninvasive Diagnosis of Small Bowel Crohn’s Disease: Direct Comparison of Bowel Sonography and Magnetic Resonance Enterography. Inflammatory Bowel Diseases. 2013;19(5):991-998. doi:10.1097/MIB.0b013e3182802b87
19. Pallotta N, Civitelli F, Di Nardo G, et al. Small Intestine Contrast Ultrasonography in Pediatric Crohn’s Disease. The Journal of Pediatrics. 2013;163(3):778-784.e1. doi:10.1016/j.jpeds.2013.03.056
20. Rispo A, de Sire R, Mainenti PP, et al. David Against Goliath: Direct Comparison of Handheld Bowel Sonography and Magnetic Resonance Enterography for Diagnosis of Crohn’s Disease. Inflammatory Bowel Diseases. Published online June 6, 2022:izac116. doi:10.1093/ibd/izac116
21. Calabrese E, Maaser C, Zorzi F, et al. Bowel Ultrasonography in the Management of Crohnʼs Disease. A Review with Recommendations of an International Panel of Experts: Inflammatory Bowel Diseases. 2016;22(5):1168-1183. doi:10.1097/MIB.0000000000000706
22. Taylor SA, Mallett S, Bhatnagar G, 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. The Lancet Gastroenterology & Hepatology. 2018;3(8):548-558. doi:10.1016/S2468-1253(18)30161-4
23. Reimund JM, Jung-Chaigneau E, Chamouard P, Wittersheim C, Duclos B, Baumann R. [Diagnostic value of high resolution sonography in Crohn’s disease and ulcerative colitis]. Gastroenterol Clin Biol. 1999;23(6-7):740-746.
24. Bru C, Sans M, Defelitto MM, et al. Hydrocolonic Sonography for Evaluating Inflammatory Bowel Disease. American Journal of Roentgenology. 2001;177(1):99-105. doi:10.2214/ajr.177.1.1770099
25. Parente F, Greco S, Molteni M, et al. Role of early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel: BOWEL ULTRASOUND FOR DETECTION OF INFLAMMATORY DISEASE. Alimentary Pharmacology & Therapeutics. 2003;18(10):1009-1016. doi:10.1046/j.1365-2036.2003.01796.x
26. Parente F. 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(11):1652-1657. doi:10.1136/gut.2004.041038
27. Martínez MJ, Ripollés T, Paredes JM, Blanc E, Martí-Bonmatí L. Assessment of the extension and the inflammatory activity in Crohn’s disease: comparison of ultrasound and MRI. Abdom Imaging. 2009;34(2):141-148. doi:10.1007/s00261-008-9365-y
28. Rispo A, Imperatore N, Testa A, et al. Bowel Damage in Crohnʼs Disease: Direct Comparison of Ultrasonography-based and Magnetic Resonance-based Lemann Index. Inflammatory Bowel Diseases. 2017;23(1):143-151. doi:10.1097/MIB.0000000000000980
29. Allocca M, Fiorino G, Bonifacio C, et al. Comparative Accuracy of Bowel Ultrasound Versus Magnetic Resonance Enterography in Combination With Colonoscopy in Assessing Crohn’s Disease and Guiding Clinical Decision-making. Journal of Crohn’s and Colitis. 2018;12(11):1280-1287. doi:10.1093/ecco-jcc/jjy093
30. Panés J, Bouzas R, Chaparro M, 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: Systematic review: cross-sectional imaging in Crohn’s disease. Alimentary Pharmacology & Therapeutics. 2011;34(2):125-145. doi:10.1111/j.1365-2036.2011.04710.x
31. Calabrese E, La Seta F, Buccellato A, et al. Crohnʼs Disease: A Comparative Prospective Study of Transabdominal Ultrasonography, Small Intestine Contrast Ultrasonography, and Small Bowel Enema: Inflammatory Bowel Diseases. 2005;11(2):139-145. doi:10.1097/00054725-200502000-00007
32. Ismail MS, Charabaty A. Management of Crohn’s stricture: medical, endoscopic and surgical therapies. Frontline Gastroenterol. 2022;13(6):524-530. doi:10.1136/flgastro-2021-101827
33. Gasche C, Moser G, Turetschek K, Schober E, Moeschl P, Oberhuber G. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut. 1999;44(1):112-117. doi:10.1136/gut.44.1.112
34. Kohn A, Cerro P, Milite G, De Angelis E, Prantera C. Prospective Evaluation of Transabdominal Bowel Sonography in the Diagnosis of Intestinal Obstruction in Crohnʼs Disease: Comparison with Plain Abdominal Film and Small Bowel Enteroclysis: Inflammatory Bowel Diseases. 1999;5(3):153-157. doi:10.1097/00054725-199908000-00001
35. Pallotta N, Vincoli G, Montesani C, et al. Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in crohnʼs disease: A prospective comparative study versus intraoperative findings: Inflammatory Bowel Diseases. 2012;18(1):74-84. doi:10.1002/ibd.21678
36. Onali S. Small intestine contrast ultrasonography vs computed tomography enteroclysis for assessing ileal Crohn’s disease. WJG. 2012;18(42):6088. doi:10.3748/wjg.v18.i42.6088
37. Kumar S, Hakim A, Alexakis C, et al. Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn’s disease: Correlation with intraoperative findings and magnetic resonance enterography: Small intestinal contrast ultrasonography in Crohn’s disease. J Gastroenterol Hepatol. 2015;30(1):86-91. doi:10.1111/jgh.12724
38. Maconi G, Sampietro GM, Parente F, et al. Contrast Radiology, Computed Tomography and Ultrasonography in Detecting Internal Fistulas and Intra-Abdominal Abscesses in Crohn’s Disease: A Prospective Comparative Study. American Journal of Gastroenterology. 2003;98(7):1545-1555. doi:10.1111/j.1572-0241.2003.07521.x
39. Grażyńska A, Kufel J, Dudek A, Cebula M. Shear Wave and Strain Elastography in Crohn’s Disease—A Systematic Review. Diagnostics. 2021;11(9):1609. doi:10.3390/diagnostics11091609
40. Torres J, Mehandru S, Colombel JF, Peyrin-Biroulet L. Crohn’s disease. The Lancet. 2017;389(10080):1741-1755. doi:10.1016/S0140-6736(16)31711-1
41. Adamina M, Bonovas S, Raine T, et al. ECCO Guidelines on Therapeutics in Crohn’s Disease: Surgical Treatment. Journal of Crohn’s and Colitis. 2020;14(2):155-168. doi:10.1093/ecco-jcc/jjz187
42. Rispo A, Imperatore N, Testa A, et al. Diagnostic Accuracy of Ultrasonography in the Detection of Postsurgical Recurrence in Crohn’s Disease: A Systematic Review with Meta-analysis. Inflammatory Bowel Diseases. 2018;24(5):977-988. doi:10.1093/ibd/izy012
43. Andreoli A, Prantera C. Role of Ultrasonography in the Diagnosis of Postsurgical Recurrence of Crohn’s Disease. 1998;93(7).
44. Rispo A, Bucci L, Pesce G, et al. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohnʼs disease: Inflammatory Bowel Diseases. 2006;12(6):486-490. doi:10.1097/00054725-200606000-00007
45. Castiglione F, Bucci L, Pesce G, et al. Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohnʼs disease: Inflammatory Bowel Diseases. 2008;14(9):1240-1245. doi:10.1002/ibd.20469
46. Calabrese E, Petruzziello C, Onali S, et al. Severity of postoperative recurrence in crohnʼs disease: Correlation between endoscopic and sonographic findings: Inflammatory Bowel Diseases. 2009;15(11):1635-1642. doi:10.1002/ibd.20948
47. Onali S, Calabrese E, Petruzziello C, et al. Post-operative recurrence of Crohn’s disease: A prospective study at 5 years. Digestive and Liver Disease. 2016;48(5):489-494. doi:10.1016/j.dld.2016.01.009
48. Dal Piaz G, Mendolaro M, Mineccia M, et al. Predictivity of early and late assessment for post-surgical recurrence of Crohn’s disease: Data from a single-center retrospective series. Digestive and Liver Disease. 2021;53(8):987-995. doi:10.1016/j.dld.2020.09.018
49. S. Hollerbach, A. Geissler, H. Schi. The Accuracy of Abdominal Ultrasound in the Assessment of Bowel Disorders. Scandinavian Journal of Gastroenterology. 1998;33(11):1201-1208. doi:10.1080/00365529850172575
50. Truong M, Atri M, Bret PM, et al. Sonographic appearance of benign and malignant conditions of the colon. American Journal of Roentgenology. 1998;170(6):1451-1455. doi:10.2214/ajr.170.6.9609152
51. Lim JH, Ko YT, Lee DH, Lim JW, Kim TH. Sonography of inflammatory bowel disease: findings and value in differential diagnosis. American Journal of Roentgenology. 1994;163(2):343-347. doi:10.2214/ajr.163.2.8037027
52. Schwerck W, Beckh K, Raith M. A prospective evaluation of high resolution sonography in the diagnosis of inflammatory bowel disease.
53. Allocca M, Fiorino G, Bonovas S, et al. Accuracy of Humanitas Ultrasound Criteria in Assessing Disease Activity and Severity in Ulcerative Colitis: A Prospective Study. Journal of Crohn’s and Colitis. 2018;12(12):1385-1391. doi:10.1093/ecco-jcc/jjy107
54. Kinoshita K, Katsurada T, Nishida M, et al. Usefulness of transabdominal ultrasonography for assessing ulcerative colitis: a prospective, multicenter study. J Gastroenterol. 2019;54(6):521-529. doi:10.1007/s00535-018-01534-w
55. Sagami S, Kobayashi T, Miyatani Y, et al. Accuracy of Ultrasound for Evaluation of Colorectal Segments in Patients With Inflammatory Bowel Diseases: A Systematic Review and Meta-analysis. Clinical Gastroenterology and Hepatology. 2021;19(5):908-921.e6. doi:10.1016/j.cgh.2020.07.067
56. Bozkurt T, Rommel T, Stabenow-Lohbauer U, Langer M, Schmiegelow P, Lux G. Sonographic bowel wall morphology correlates with clinical and endoscopic activity in crohn’s disease and ulcerative colitis. European Journal of Ultrasound. 1996;4(1):27-33. doi:10.1016/0929-8266(95)00169-7
57. Antonelli E, Giuliano V, Casella G, et al. Ultrasonographic assessment of colonic wall in moderate–severe ulcerative colitis: Comparison with endoscopic findings. Digestive and Liver Disease. 2011;43(9):703-706. doi:10.1016/j.dld.2011.02.019
58. Allocca M, Filippi E, Costantino A, et al. Milan ultrasound criteria are accurate in assessing disease activity in ulcerative colitis: external validation. United European Gastroenterol j. 2021;9(4):438-442. doi:10.1177/2050640620980203
59. Bots S, Nylund K, Löwenberg M, Gecse K, D’Haens G. Intestinal Ultrasound to Assess Disease Activity in Ulcerative Colitis: Development of a novel UC-Ultrasound Index. Journal of Crohn’s and Colitis. 2021;15(8):1264-1271. doi:10.1093/ecco-jcc/jjab002
60. Fraquelli M, Sarno A, Girelli C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn’s disease. Digestive and Liver Disease. 2008;40(11):860-866. doi:10.1016/j.dld.2008.04.006
61. De Voogd F, Wilkens R, Gecse K, et al. A Reliability Study: Strong Inter-Observer Agreement of an Expert Panel for Intestinal Ultrasound in Ulcerative Colitis. Journal of Crohn’s and Colitis. 2021;15(8):1284-1290. doi:10.1093/ecco-jcc/jjaa267
62. Novak KL, Nylund K, Maaser C, 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. Journal of Crohn’s and Colitis. 2021;15(4):609-616. doi:10.1093/ecco-jcc/jjaa216
63. Allocca M, Craviotto V, Dell’Avalle C, et al. Bowel ultrasound score is accurate in assessing response to therapy in patients with Crohn’s disease. Aliment Pharmacol Ther. 2022;55(4):446-454. doi:10.1111/apt.16700
64. Allocca M, Dell’Avalle C, Craviotto V, et al. Predictive value of Milan ultrasound criteria in ulcerative colitis: A prospective observational cohort study. UEG Journal. 2022;10(2):190-197. doi:10.1002/ueg2.12206
65. Mjolstad OC, Dalen H, Graven T, Kleinau JO, Salvesen O, Haugen BO. Routinely adding ultrasound examinations by pocket-sized ultrasound devices improves inpatient diagnostics in a medical department. European Journal of Internal Medicine. 2012;23(2):185-191. doi:10.1016/j.ejim.2011.10.009
66. Wastl D, Löwe A, Dietrich CF. Echoscopy in scanning abdominal diseases in a critical care setting. Med Klin Intensivmed Notfmed. Published online June 2, 2022. doi:10.1007/s00063-022-00926-4
67. Barreiros A, Cui X, Ignee A, De Molo C, Pirri C, Dietrich C. EchoScopy in Scanning Abdominal Diseases: Initial Clinical Experience. Z Gastroenterol. 2014;52(03):269-275. doi:10.1055/s-0033-1350114
68. Testuz A, Muller H, Keller PF, et al. Diagnostic accuracy of pocket-size handheld echocardiographs used by cardiologists in the acute care setting. European Heart Journal - Cardiovascular Imaging. 2013;14(1):38-42. doi:10.1093/ehjci/jes085
69. Rispo A, Calabrese G, Testa A, et al. Hocus Pocus: the Role of Hand-held Ultrasonography in Predicting Disease Extension and Endoscopic Activity in Ulcerative Colitis. Journal of Crohn’s and Colitis. Published online February 16, 2023:jjad024. doi:10.1093/ecco-jcc/jjad024