Clinical Ultrasound in Inflammatory Bowel Disease

Abstract

Ultrasound should be the first-line imaging method in the medical care of patients with inflammatory bowel disease. It can be used to differentiate between Crohn’s disease and ulcerative colitis and to detect numerous complications like stenoses, fistulas, and abscesses. As the method is also highly suitable for follow-up, stressful endoscopic procedures and examinations involving radiation are less necessary. Comparison studies with MRI and CT show that ultrasound is not an inferior method and it is therefore included in all guidelines. Intensifying physician training in this method will help to ensure its comprehensive use.

Zusammenfassung

Bei der Betreuung von CED-Patienten ist die Sonografie das als erstes anzuwendende bildgebende Verfahren. Mit ihrer Hilfe ist häufig eine Unterscheidung zwischen dem M. Crohn und der Colitis ulcerosa möglich und es können zahlreiche Komplikationen wie Stenosen, Fisteln und Abszesse erkannt werden. Auch zur Verlaufsbeurteilung ist die Methode hervorragend geeignet. Mit ihrer Hilfe können hier endoskopische und strahlenbelastende Untersuchungen eingespart werden. In Vergleichsstudien mit MRT und CT ist der Ultraschall nicht unterlegen, deshalb findet er sich auch in allen Leitlinien wieder. Durch eine Intensivierung der Ausbildung von Ärzten sollte diesem Verfahren zu einer flächendeckenden Anwendung verholfen werden.

• References

• 1 Crohn BB. REGIONAL ILEITIS. JAMA 1932; 99: 1323 . DOI:10.1001/jama.1932.02740680019005
• 2 Ye Y, Pang Z, Chen W. et al. The epidemiology and risk factors of inflammatory bowel disease. International journal of clinical and experimental medicine 2015; 8: 22529-22542
• 3 Malmborg P, Hildebrand H. The emerging global epidemic of paediatric inflammatory bowel disease – causes and consequences. Journal of internal medicine 2016; 279: 241-258 . DOI:10.1111/joim.12413
• 4 Korzenik JR. Past and current theories of etiology of IBD: toothpaste, worms, and refrigerators. Journal of clinical gastroenterology 2005; 39: S59-S65
• 5 Abraham C, Cho JH. Inflammatory bowel disease. The New England journal of medicine 2009; 361: 2066-2078 . DOI:10.1056/NEJMra0804647
• 6 Lees CW, Satsangi J. Genetics of inflammatory bowel disease: implications for disease pathogenesis and natural history. Expert review of gastroenterology & hepatology 2009; 3: 513-534 . DOI:10.1586/egh.09.45
• 7 Danese S, Fiocchi C. Ulcerative colitis. The New England journal of medicine 2011; 365: 1713-1725 . DOI:10.1056/NEJMra1102942
• 8 Nylund K, Maconi G, Hollerweger A. et al. EFSUMB-Empfehlungen und Leitlinien des Gastrointestinalen Ultraschalls – Teil 1: Untersuchungstechniken und Normalbefund (Langversion). Ultraschall in Med (Stuttgart, Germany 1980) 2017; 38: e1-e15 . DOI:10.1055/s-0042-115853
• 9 Worlicek H, Dunz D, Engelhard K. Ultrasonic examination of the wall of the fluid-filled stomach. J Clin Ultrasound 1989; 17: 5-14 . DOI:10.1002/jcu.1870170103
• 10 Mocci G, Migaleddu V, Cabras F. et al. SICUS and CEUS imaging in Crohn’s disease: An update. Journal of ultrasound 2017; 20: 1-9 . DOI:10.1007/s40477-016-0230-5
• 11 Limberg B. Hydrokolonsonographie – Möglichkeiten und Grenzen einer sonographischen Diagnostik von Dickdarmerkrankungen. Zeitschrift für Gastroenterologie 2001; 39: 1007-1015 . DOI:10.1055/s-2001-19020
• 12 Lutz H, Bauer U, Stolte M. Ultrasound diagnosis of the stomach wall--experimental studies. Ultraschall in Med (Stuttgart, Germany 1980) 1986; 7: 255-258 . DOI:10.1055/s-2007-1013961
• 13 Kimmey MB, Martin RW, Haggitt RC. et al. Histologic correlates of gastrointestinal ultrasound images. Gastroenterology 1989; 96: 433-441
• 14 Ødegaard S, Nesje LB, Lærum OD. et al. High-frequency ultrasonographic imaging of the gastrointestinal wall. Expert review of medical devices 2012; 9: 263-273 . DOI:10.1586/erd.12.6
• 15 Lutz HT, Petzoldt R. Ultrasonic patterns of space occupying lesions of the stomach and the intestine. Ultrasound in Medicine & Biology 1976; 2: 129-132 . DOI:10.1016/0301-5629(76)90022-3
• 16 Rettenmaier G. Sonographische Zeichen der pathologischen Magenwandverdickung. Ultraschall in Med 1980; 1: 26-34 . DOI:10.1055/s-2007-1010132
• 17 Seitz K. Sonographische Diagnostik beim Morbus Crohn. Ultraschall in Med 1980; 1: 35-40 . DOI:10.1055/s-2007-1010133
• 18 Meckler U, Herzog P. Sonographic structure of the intestinal wall--significance for the diagnosis of inflammatory intestinal diseases. Ultraschall inMed (Stuttgart, Germany 1980) 1989; 10: 152-157 . DOI:10.1055/s-2007-1005982
• 19 Hollerweger A, Dietrich CF. White Bowel. A Sonographic Sign of intestinal lymph edema?. Ultraschall in Med 2005; 2: 127-133
• 20 Worlicek H, Lutz H, Thoma B. Sonography of chronic inflammatory bowel diseases--a prospective study. Ultraschall in Med (Stuttgart, Germany 1980) 1986; 7: 275-280 . DOI:10.1055/s-2007-1013965
• 21 Carnevale Maffè G, Brunetti L, Formagnana P. et al. Ultrasonographic findings in Crohn’s disease. Journal of ultrasound 2015; 18: 37-49 . DOI:10.1007/s40477-014-0096-3
• 22 Holt S, Samuel E. Grey scale ultrasound in Crohn’s disease. Gut 1979; 20: 590-595
• 23 Wellmann W, Gebel M, Freise J. et al. Ultrasound in the diagnosis of ileitis terminalis Crohn (author’s transl). RoFo Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin 1980; 133: 146-148 . DOI:10.1055/s-2008-1056694
• 24 Seitz K, Reuss J. Sonographische Fisteldarstellung bei Morbus Crohn. Ultraschall in Med (Stuttgart, Germany 1980) 1986; 7: 281-283 . DOI:10.1055/s-2007-1013966
• 25 Meckler U, Caspary WF, Clement T. et al. Sonografie beim Morbus Crohn--Stellungnahme einer Expertengruppe. Zeitschrift für Gastroenterologie 1991; 29: 355-359
• 26 Limberg B. Diagnostik von chronisch-entzündlichen Darmerkrankungen durch Sonographie. Zeitschrift für Gastroenterologie 1999; 37: 495-508
• 27 Park SH, Loftus EV, Yang SK. Appendiceal skip inflammation and ulcerative colitis. Digestive diseases and sciences 2014; 59: 2050-2057 . DOI:10.1007/s10620-014-3129-z
• 28 Maconi G, Parente F, Bollani S. et al. Factors affecting splanchnic haemodynamics in Crohn’s disease: A prospective controlled study using Doppler ultrasound. Gut 1998; 43: 645-650
• 29 van Oostayen JA, Wasser MN, van Hogezand RA. et al. Doppler sonography evaluation of superior mesenteric artery flow to assess Crohn’s disease activity: Correlation with clinical evaluation, Crohn’s disease activity index, and alpha 1-antitrypsin clearance in feces. American journal of roentgenology 1997; 168: 429-433 . DOI:10.2214/ajr.168.2.9016220
• 30 Ludwig D, Wiener S, Brüning A. et al. Mesenteric blood flow is related to disease activity and risk of relapse in Crohn’s disease: A prospective follow-up study. The American journal of gastroenterology 1999; 94: 2942-2950 . DOI:10.1111/j.1572-0241.1999.01442.x
• 31 Kratzer W, Foeller T, Kaechele V. et al. Darmwandvaskularisation bei Morbus Crohn. Zeitschrift fur Gastroenterologie 2004; 42: 973-978 . DOI:10.1055/s-2004-813352
• 32 Drews BH, Barth TFE, Hänle MM. et al. Comparison of sonographically measured bowel wall vascularity, histology, and disease activity in Crohn’s disease. European radiology 2009; 19: 1379-1386 . DOI:10.1007/s00330-008-1290-5
• 33 Brahme F, Lindström C. A comparative radiographic and pathological study of intestinal vaso-architecture in Crohn’s disease and in ulcerative colitis. Gut 1970; 11: 928-940
• 34 Kalima TV, Peltokallio P, Myllärniemi H. Vascular pattern in ileal Crohn’s disease. Annals of clinical research 1975; 7: 23-31
• 35 Furukawa A, Saotome T, Yamasaki M. et al. Cross-sectional imaging in Crohn disease. Radiographics a review publication of the Radiological Society of North America, Inc 2004; 24: 689-702 . DOI:10.1148/rg.243035120
• 36 Weiss D, van der Weg B, Frenzer A. Prospective Study of Contrast enhanced ultrasound (CEUS) in Patients with Crohn’s Disease. Jahreskongress Schweizerische Gesellschaft für Gastroenterologie 2011
• 37 Ripollés T, Martínez-Pérez MJ, Blanc E. et al. Contrast-enhanced ultrasound (CEUS) in Crohn’s disease: Technique, image interpretation and clinical applications. Insights into imaging 2011; 2: 639-652 . DOI:10.1007/s13244-011-0124-1
• 38 Girlich C, Schacherer D, Jung EM. et al. 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. European journal of radiology 2012; 81: 1105-1109 . DOI:10.1016/j.ejrad.2011.02.054
• 39 Malagò R, D’Onofrio M, Mantovani W. et al. Contrast-enhanced ultrasonography (CEUS) vs. MRI of the small bowel in the evaluation of Crohn’s disease activity. La Radiologia medica 2012; 117: 268-281 . DOI:10.1007/s11547-011-0783-5
• 40 de Franco A, Marzo M, Felice C. et al. Ileal Crohn’s disease: CEUS determination of activity. Abdominal imaging 2012; 37: 359-368 . DOI:10.1007/s00261-011-9831-9
• 41 Saevik F, Nylund K, Hausken T. et al. Bowel perfusion measured with dynamic contrast-enhanced ultrasound predicts treatment outcome in patients with Crohn’s disease. Inflammatory bowel diseases 2014; 20: 2029-2037 . DOI:10.1097/MIB.0000000000000159
• 42 Romanini L, Passamonti M, Navarria M. et al. Quantitative analysis of contrast-enhanced ultrasonography of the bowel wall can predict disease activity in inflammatory bowel disease. European journal of radiology 2014; 83: 1317-1323 . DOI:10.1016/j.ejrad.2014.05.012
• 43 Liu C, Xu XR, Xu HX. et al. Conventional ultrasound and contrast-enhanced ultrasound in evaluating the severity of Crohn’s disease. International journal of clinical and experimental medicine 2015; 8: 123-134
• 44 Wilkens R, Peters DA, Nielsen AH. et al. Dynamic Contrast-Enhanced Magnetic Resonance Enterography and Dynamic Contrast-Enhanced Ultrasonography in Crohn’s Disease: An Observational Comparison Study. Ultrasound international open 2017; 3: E13-E24 . DOI:10.1055/s-0042-123841
• 45 Zink F, Kratzer W, Schmidt S. et al. Comparison of Two High-End Ultrasound Systems for Contrast-Enhanced Ultrasound Quantification of Mural Microvascularity in Crohn’s Disease. Ultraschall in Med (Stuttgart, Germany 1980) 2016; 37: 74-81 . DOI:10.1055/s-0034-1398746
• 46 Giannetti A, Biscontri M, Matergi M. Feasibility of real-time strain elastography in colonic diseases. Journal of ultrasound 2014; 17: 321-330 . DOI:10.1007/s40477-014-0124-3
• 47 Cosgrove D, Piscaglia F, Bamber J. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall in Med (Stuttgart, Germany 1980) 2013; 34: 238-253 . DOI:10.1055/s-0033-1335375
• 48 Havre R, Gilja OH. Elastography and strain rate imaging of the gastrointestinal tract. European journal of radiology 2014; 83: 438-441 . DOI:10.1016/j.ejrad.2013.05.018
• 49 Lee EH, Yang HR, Kim JY. Comparison of Transperianal Ultrasound With Colonoscopy and Magnetic Resonance Imaging in Perianal Crohn Disease. Journal of pediatric gastroenterology and nutrition 2018; 66: 614-619 . DOI:10.1097/MPG.0000000000001752
• 50 Palascak-Juif V, Bouvier AM, Cosnes J. et al. Small bowel adenocarcinoma in patients with Crohn’s disease compared with small bowel adenocarcinoma de novo. Inflammatory bowel diseases 2005; 11: 828-832
• 51 Alexander C, Reese G. von Roon. et al. The risk of cancer in patients with Crohn’s disease. Diseases of the colon and rectum 2007; 50: 839-855 . DOI:10.1007/s10350-006-0848-z
• 52 Annese V, Beaugerie L, Egan L. et al. European Evidence-based Consensus: Inflammatory Bowel Disease and Malignancies. Journal of Crohn’s & colitis 2015; 9 (11) 945-965 . DOI:10.1093/ecco-jcc/jjv141
• 53 Beaugerie L, Itzkowitz SH. Cancers complicating inflammatory bowel disease. The New England journal of medicine 2015; 372: 1441-1452 . DOI:10.1056/NEJMra1403718
• 54 Bongartz T, Sutton AJ, Sweeting MJ. et al. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA 2006; 295: 2275-2285 . DOI:10.1001/jama.295.19.2275
• 55 Mercer LK, Lunt M, Low ALS. et al. Risk of solid cancer in patients exposed to anti-tumour necrosis factor therapy: Results from the British Society for Rheumatology Biologics Register for Rheumatoid Arthritis. Annals of the rheumatic diseases 2015; 74: 1087-1093 . DOI:10.1136/annrheumdis-2013-204851
• 56 Calip GS, Patel PR, Adimadhyam S. et al. Tumor necrosis factor-alpha inhibitors and risk of non-Hodgkin lymphoma in a cohort of adults with rheumatologic conditions. International journal of cancer 2018;
• 57 Schmidt T, Reinshagen M, Brambs HJ. et al. Vergleich von Darmwandsonographie, Enteroklysma und Magnetresonanztomographie in der Erkennung von Darmwandveränderungen und Komplikationen im Dünndarm bei Patienten mit M. Crohn. Zeitschrift fur Gastroenterologie 2003; 41: 641-648 . DOI:10.1055/s-2003-40547
• 58 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. Alimentary pharmacology & therapeutics 2011; 34: 125-145 . DOI:10.1111/j.1365-2036.2011.04710.x
• 59 Stasi C, Falchini M, Milani S. Imaging modalities for the noninvasive assessment of fibrosis in Crohn’s disease. The Scientific World Journal 2012; 2012: 450151 . DOI:10.1100/2012/450151
• 60 Dillman JR, Smith EA, Sanchez RJ. et al. Pediatric Small Bowel Crohn Disease: Correlation of US and MR Enterography. Radiographics a review publication of the Radiological Society of North America, Inc 2015; 35: 835-848 . DOI:10.1148/rg.2015140002
• 61 Maconi G, Nylund K, Ripolles T. et al. EFSUMB-Empfehlungen und klinische Leitlinien für den gastrointestinalen Ultraschall (GIUS) chronisch entzündlichen Darmerkrankungen (CED). Ultraschall in Med (Stuttgart, Germany 1980) 2018;
• 62 Mathews JD, Forsythe AV, Brady Z. et al. Cancer risk in 680 000 people exposed to computed tomography scans in childhood or adolescence: Data linkage study of 11 million Australians. BMJ (Clinical research ed.) 2013; 346: f2360 . DOI:10.1136/bmj.f2360
• 63 Estay C, Simian D, Lubascher J. et al. Ionizing radiation exposure in patients with inflammatory bowel disease: are we overexposing our patients?. Journal of digestive diseases 2015; 16: 83-89 . DOI:10.1111/1751-2980.12213
• 64 Brenner DJ, Hall EJ. Computed tomography--an increasing source of radiation exposure. The New England journal of medicine 2007; 357: 2277-2284 . DOI:10.1056/NEJMra072149
• 65 Smith-Bindman R. Is computed tomography safe?. The New England journal of medicine 2010; 363: 1-4 . DOI:10.1056/NEJMp1002530
• 66 Hillman BJ, Goldsmith JC. The uncritical use of high-tech medical imaging. The New England journal of medicine 2010; 363: 4-6 . DOI:10.1056/NEJMp1003173
• 67 Gionchetti P, Dignass A, Danese S. et al. 3rd European Evidence-based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 2: Surgical Management and Special Situations. Journal of Crohn’s & colitis 2017; 11: 135-149 . DOI:10.1093/ecco-jcc/jjw169
• 68 Maconi G, Tonolini M, Monteleone M. et al. Transperineal perineal ultrasound versus magnetic resonance imaging in the assessment of perianal Crohn’s disease. Inflammatory bowel diseases 2013; 19: 2737-2743 . DOI:10.1097/01.MIB.0000436274.95722.e5
• 69 Terracciano F, Scalisi G, Bossa F. et al. Transperineal ultrasonography: First level exam in IBD patients with perianal disease. Digestive and liver disease official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver 2016; 48: 874-879 . DOI:10.1016/j.dld.2016.03.027
• 70 Hwang JY, Yoon HK, Kim WK. et al. Transperineal ultrasonography for evaluation of the perianal fistula and abscess in pediatric Crohn disease: Preliminary study. Ultrasonography (Seoul, Korea) 2014; 33: 184-190 . DOI:10.14366/usg.14009
• 71 Gaspar SR, Mendonça T, Oliveira P. et al. Urolithiasis and crohn’s disease. Urology annals 2016; 8: 297-304 . DOI:10.4103/0974-7796.184879
• 72 Abbas G, Lindor KD. Cholangiocarcinoma in primary sclerosing cholangitis. Journal of gastrointestinal cancer 2009; 40: 19-25 . DOI:10.1007/s12029-009-9085-8
• 73 Lazaridis KN, LaRusso NF. Primary Sclerosing Cholangitis. The New England journal of medicine 2016; 375: 1161-1170 . DOI:10.1056/NEJMra1506330
• 74 Pitchumoni CS, Rubin A, Das K. Pancreatitis in inflammatory bowel diseases. Journal of clinical gastroenterology 2010; 44: 246-253 . DOI:10.1097/MCG.0b013e3181cadbe1
• 75 Mauch M, Blank W, Kunze G. et al. Importance of Abdominal Ultrasound in 17 Patients with Histologically Confirmed Autoimmune Pancreatitis (AIP). Ultraschall in Med (Stuttgart, Germany 1980) 2015; 36: 248-254 . DOI:10.1055/s-0034-1385385
• 76 Papay P, Ignjatovic A, Karmiris K. et al. Optimising monitoring in the management of Crohn’s disease: A physician’s perspective. Journal of Crohn’s and Colitis 2013; 7: 653-669 . DOI:10.1016/j.crohns.2013.02.005
• 77 Gomollón F, Dignass A, Annese V. et al. 3rd European Evidence-based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 1: Diagnosis and Medical Management. Journal of Crohn’s & colitis 2017; 11: 3-25 . DOI:10.1093/ecco-jcc/jjw168
• 78 Preiß JC, Bokemeyer B, Buhr HJ. et al. Aktualisierte S3-Leitlinie--„Diagnostik und Therapie des Morbus Crohn“ 2014. Zeitschrift fur Gastroenterologie 2014; 52: 1431-1484
• 79 Dillman JR, Stidham RW, Higgins PDR. et al. US elastography-derived shear wave velocity helps distinguish acutely inflamed from fibrotic bowel in a Crohn disease animal model. Radiology 2013; 267: 757-766 . DOI:10.1148/radiol.13121775
• 80 Baumgart DC, Müller HP, Grittner U. et al. US-based Real-time Elastography for the Detection of Fibrotic Gut Tissue in Patients with Stricturing Crohn Disease. Radiology 2015; 275: 889-899 . DOI:10.1148/radiol.14141929
• 81 Ripollés T, Rausell N, Paredes JM. et al. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn’s disease: a comparison with surgical histopathology analysis. Journal of Crohn’s & colitis 2013; 7: 120-128 . DOI:10.1016/j.crohns.2012.03.002
• 82 Bettenworth D, Nowacki TM, Cordes F. et al. Assessment of stricturing Crohn’s disease: Current clinical practice and future avenues. World journal of gastroenterology 2016; 22: 1008-1016 . DOI:10.3748/wjg.v22.i3.1008
• 83 Nylund K, Sævik F, Leh S. et al. Interobserver-Analyse der CEUS abgeleiteten Perfusion bei fibrotischem und entzündlichem Morbus Crohn. Ultraschall in Med (Stuttgart, Germany 1980) 2018;
• 84 Pita I, Magro F. Advanced imaging techniques for small bowel Crohn’s disease: What does the future hold?. Therapeutic advances in gastroenterology 2018; 11
• 85 Quaia E, Gennari AG, Cova MA. et al. 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 in Medicine & Biology 2018; 44: 762-770 . DOI:10.1016/j.ultrasmedbio.2017.11.015
• 86 Lenze F, Wessling J, Bremer J. et al. Detection and differentiation of inflammatory versus fibromatous Crohn’s disease strictures: Prospective comparison of 18F-FDG-PET/CT, MR-enteroclysis, and transabdominal ultrasound versus endoscopic/histologic evaluation. Inflammatory bowel diseases 2012; 18: 2252-2260 . DOI:10.1002/ibd.22930
• 87 Rimola J, Planell N, Rodríguez S. et al. Characterization of inflammation and fibrosis in Crohn’s disease lesions by magnetic resonance imaging. The American journal of gastroenterology 2015; 110: 432-440 . DOI:10.1038/ajg.2014.424
• 88 Maio G. Medicine and the holistic understanding of the human being: Ultrasound examination as dialog. Ultraschall in Med (Stuttgart, Germany 1980) 2014; 35: 98-107 . DOI:10.1055/s-0034-1366182
• 89 Maconi G, Bolzoni E, Giussani A. et al. Accuracy and cost of diagnostic strategies for patients with suspected Crohn’s disease. Journal of Crohn’s & colitis 2014; 8: 1684-1692 . DOI:10.1016/j.crohns.2014.08.005
• 90 Novak K, Tanyingoh D, Petersen F. et al. Clinic-based Point of Care Transabdominal Ultrasound for Monitoring Crohn’s Disease: Impact on Clinical Decision Making. Journal of Crohn’s & colitis 2015; 9: 795-801 . DOI:10.1093/ecco-jcc/jjv105
• 91 Conti CB, Giunta M, Gridavilla D. et al. Role of Bowel Ultrasound in the Diagnosis and Follow-up of Patients with Crohn’s Disease. Ultrasound in Medicine & Biology 2017; 43: 725-734 . DOI:10.1016/j.ultrasmedbio.2016.12.014
• 92 Kucharzik T, Wittig BM, Helwig U. et al. Use of Intestinal Ultrasound to Monitor Crohn’s Disease Activity. Clinical gastroenterology and hepatology the official clinical practice journal of the American Gastroenterological Association 2017; 15: 535-542.e2 . DOI:10.1016/j.cgh.2016.10.040