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Evolving roles of cross-sectional imaging in Crohn's disease

      Abstract

      The implementation of cross-sectional imaging techniques for the clinical management of Crohn's disease patients has steadily grown over the recent years, thanks to a series of technological advances, including the evolution of contrast media for magnetic resonance, computed tomography and bowel ultrasound. This has resulted in a continuous improvement of diagnostic accuracy and capability to detect Crohn's disease-related complications. Additionally, a progressive widening of indications for cross-sectional imaging in Crohn's disease has been put forward, thus leading to hypothesize that in the near future imaging techniques can increasingly complement endoscopy in most clinical settings, including the grading of disease activity and the assessment of mucosal healing or Crohn's disease post-surgical recurrence.

      Keywords

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      References

        • Thia K.T.
        • Sandborn W.J.
        • Harmsen W.S.
        • et al.
        Risk factors associated with progression to intestinal complications of Crohn's disease in a population-based cohort.
        Gastroenterology. 2010; 139: 1147-1155
        • Grand D.J.
        • Harris A.
        • Loftus Jr., E.V.
        Imaging for luminal disease and complications: CT enterography, MR enterography, small-bowel follow-through, and ultrasound.
        Gastroenterology Clinics of North America. 2012; 41: 497-512
        • 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 and Therapeutics. 2011; 34: 125-145
        • Quaia E.
        • Cabibbo B.
        • Sozzi M.
        • et al.
        Biochemical markers and MR imaging findings as predictors of Crohn disease activity in patients scanned by contrast-enhanced MR enterography.
        Academic Radiology. 2014; 21: 1225-1232
        • Denis M.A.
        • Reenaers C.
        • Fontaine F.
        • et al.
        Assessment of endoscopic activity index and biological inflammatory markers in clinically active Crohn's disease with normal C-reactive protein serum level.
        Inflammatory Bowel Diseases. 2007; 13: 1100-1105
        • Colombel J.F.
        • Sandborn W.J.
        • Reinisch W.
        • et al.
        Infliximab, azathioprine, or combination therapy for Crohn's disease.
        New England Journal of Medicine. 2010; 362: 1383-1395
        • Peyrin-Biroulet L.
        • Reinisch W.
        • Colombel J.F.
        • et al.
        Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn's disease in the SONIC trial.
        Gut. 2014; 63: 88-95
        • Peyrin-Biroulet L.
        • Sandborn W.
        • Sands B.E.
        • et al.
        Selecting therapeutic targets in inflammatory bowel disease (STRIDE): determining therapeutic goals for treat-to-target.
        American Journal of Gastroenterology. 2015; 110: 1324-1338
        • Williet N.
        • Sandborn W.J.
        • Peyrin-Biroulet L.
        Patient-reported outcomes as primary end points in clinical trials of inflammatory bowel disease.
        Clinical Gastroenterology and Hepatology. 2014; 12: 1246-1256
        • Horsthuis K.
        • Bipat S.
        • Stokkers P.C.
        • et al.
        Magnetic resonance imaging for evaluation of disease activity in Crohn's disease: a systematic review.
        European Radiology. 2009; 19: 1450-1460
        • Rimola J.
        • Rodriguez S.
        • García-Bosch O.
        • et al.
        Magnetic resonance for assessment of disease activity and severity in ileocolonic Crohn's disease.
        Gut. 2009; 58: 1113-1120
        • Rimola J.
        • Ordás I.
        • Rodriguez S.
        • et al.
        Magnetic resonance imaging for evaluation of Crohn's disease: validation of parameters of severity and quantitative index of activity.
        Inflammatory Bowel Diseases. 2011; 17: 1759-1768
        • Ordás I.
        • Rimola J.
        • Rodríguez S.
        • et al.
        Accuracy of magnetic resonance enterography in assessing response to therapy and mucosal healing in patients with Crohn's disease.
        Gastroenterology. 2014; 146: 374-382
        • Coimbra A.J.
        • Rimola J.
        • O’Byrne S.
        • et al.
        Magnetic resonance enterography is feasible and reliable in multicenter clinical trials in patients with Crohn's disease, and may help select subjects with active inflammation.
        Alimentary Pharmacology and Therapeutics. 2016; 43: 61-72
        • Moseley M.E.
        • Cohen Y.
        • Mintorovitch J.
        • et al.
        Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy.
        Magnetic Resonance in Medicine. 1990; 14: 330-346
        • Kiryu S.
        • Dodanuki K.
        • Takao H.
        • et al.
        Free-breathing diffusion-weighted imaging for the assessment of inflammatory activity in Crohn's disease.
        Journal of Magnetic Resonance Imaging. 2009; 29: 880-886
        • Oto A.
        • Zhu F.
        • Kulkarni F.
        • et al.
        Evaluation of diffusion-weighted MR imaging for detection of bowel inflammation in patients with Crohn's disease.
        Academic Radiology. 2009; 16: 597-603
        • Seo N.
        • Park S.H.
        • Kim K.J.
        • et al.
        MR enterography for the evaluation of small-bowel inflammation in Crohn disease by using diffusion-weighted imaging without intravenous contrast material: a prospective noninferiority study.
        Radiology. 2015; ([Epub ahead of print])
        • Foti P.V.
        • Farina R.
        • Coronella M.
        • et al.
        Crohn's disease of the small bowel: evaluation of ileal inflammation by diffusion-weighted MR imaging and correlation with the Harvey-Bradshaw index.
        La Radiologia Medica. 2015; 120: 585-594
        • Hordonneau C.
        • Buisson A.
        • Scanzi J.
        • et al.
        Diffusion-weighted magnetic resonance imaging in ileocolonic Crohn's disease: validation of quantitative index of activity.
        American Journal of Gastroenterology. 2014; 109: 89-98
        • Parente F.
        • Maconi G.
        • Bollani S.
        • et al.
        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: 490-495
        • Maconi G.
        • Parente F.
        • Bollani S.
        • et al.
        Abdominal ultrasound in the assessment of extent and activity of Crohn's disease: clinical significance and implication of bowel wall thickening.
        American Journal of Gastroenterology. 1996; 91: 1604-1609
        • 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.
        Alimentary Pharmacology and Therapeutics. 2003; 18: 1009-1016
        • Bru C.
        • Sans M.
        • Defelitto M.M.
        • et al.
        Hydrocolonic sonography for evaluating inflammatory bowel disease.
        American Journal of Roentgenology. 2001; 177: 99-105
        • Neye H.
        • Voderholzer W.
        • Rickes S.
        • et al.
        Evaluation of criteria for the activity of Crohn's disease by power Doppler sonography.
        Digestive Diseases. 2004; 22: 67-72
        • Sasaki T.
        • Kunisaki R.
        • Kinoshita H.
        • et al.
        Doppler ultrasound findings correlate with tissue vascularity and inflammation in surgical pathology specimens from patients with small intestinal Crohn's disease.
        BMC Research Notes. 2014; 7: 363
        • Migaleddu V.
        • Scanu A.M.
        • Quaia E.
        • et al.
        Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn's disease.
        Gastroenterology. 2009; 137: 43-52
        • Limberg B.
        Diagnosis of chronic inflammatory bowel disease by ultrasonography.
        Zeitschrift fur Gastroenterologie. 1999; 37: 495-508
        • 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
        • Rieder F.
        • Zimmermann E.M.
        • Remzi F.H.
        • et al.
        Crohn's disease complicated by strictures: a systematic review.
        Gut. 2013; 62: 1072-1084
        • Chiorean M.V.
        • Sandrasegaran K.
        • Saxena R.
        • et al.
        Correlation of CT enteroclysis with surgical pathology in Crohn's disease.
        American Journal of Gastroenterology. 2007; 102: 2541-2550
        • Zappa M.
        • Stefanescu C.
        • Cazals-Hatem D.
        • et al.
        Which magnetic resonance imaging findings accurately evaluate inflammation in small bowel Crohn's disease? A retrospective comparison with surgical pathologic analysis.
        Inflammatory Bowel Diseases. 2011; 17: 984-993
        • Peyrin-Biroulet L.
        • Loftus E.V.
        • Colombel J.F.
        • et al.
        The natural history of adult Crohn's disease in population-based cohorts.
        American Journal of Gastroenterology. 2010; 105: 289-297
        • Lichtenstein G.R.
        • Olson A.
        • Travers S.
        • et al.
        Factors associated with the development of intestinal strictures or obstructions in patients with Crohn's disease.
        American Journal of Gastroenterology. 2006; 101: 1030-1038
        • Punwani S.
        • Rodriguez-Justo M.
        • Bainbridge A.
        • et al.
        Mural inflammation in Crohn disease: location-matched histologic validation of MR imaging features.
        Radiology. 2009; 252: 712-720
        • Rimola J.
        • Planell N.
        • Rodríguez S.
        • et al.
        Characterization of inflammation and fibrosis in Crohn's disease lesions by magnetic resonance imaging.
        American Journal of Gastroenterology. 2015; 110: 432-440
        • Rieder F.
        • de Bruyn J.R.
        • Pham B.T.
        • et al.
        Results of the 4th scientific workshop of the ECCO (Group II): markers of intestinal fibrosis in inflammatory bowel disease.
        Journal of Crohn's and Colitis. 2014; 8: 1166-1178
        • Tielbeek J.A.
        • Ziech M.L.
        • Li Z.
        • et al.
        Evaluation of conventional, dynamic contrast enhanced and diffusion weighted MRI for quantitative Crohn's disease assessment with histopathology of surgical specimens.
        European Radiology. 2014; 24: 619-629
        • Ziech M.L.
        • Bipat S.
        • Roelofs J.J.
        • et al.
        Retrospective comparison of magnetic resonance imaging features and histopathology in Crohn's disease patients.
        European Journal of Radiology. 2011; 80: e299-e305
        • Fornasa F.
        • Benassuti C.
        • Benazzato L.
        Role of magnetic resonance enterography in differentiating between fibrotic and active inflammatory small bowel stenosis in patients with Crohn's disease.
        Journal of Clinical Imaging Science. 2011; 1: 35
        • Lawrance I.C.
        • Welman J.C.
        • Shipman P.
        • et al.
        Correlation of MRI-determined small bowel Crohn's disease categories with medical response and surgical pathology.
        World Journal of Gastroenterology. 2009; 15: 3367-3375
        • Adler J.
        • Swanson S.D.
        • Schmiedlin-Ren P.
        • et al.
        Magnetization transfer helps detect intestinal fibrosis in an animal model of Crohn disease.
        Radiology. 2011; 259: 127-135
        • Dillman J.R.
        • Swanson S.D.
        • Johnson L.A.
        • et al.
        Comparison of noncontrast MRI magnetization transfer and T2-weighted signal intensity ratios for detection of bowel wall fibrosis in a Crohn's disease animal model.
        Journal of Magnetic Resonance Imaging. 2015; 42: 801-810
        • Pazahr S.
        • Blume I.
        • Frei P.
        • et al.
        Magnetization transfer for the assessment of bowel fibrosis in patients with Crohn's disease: initial experience.
        Magma. 2013; 26: 291-301
        • Adler J.
        • Punglia D.R.
        • Dillman J.R.
        • et al.
        Computed tomography enterography findings correlate with tissue inflammation, not fibrosis in resected small bowel Crohn's disease.
        Inflammatory Bowel Diseases. 2012; 18: 849-856
        • Quencer K.B.
        • Nimkin K.
        • Mino-Kenudson M.
        • et al.
        Detecting active inflammation and fibrosis in pediatric Crohn's disease: prospective evaluation of MR-E and CT-E.
        Abdominal Imaging. 2013; 38: 705-713
        • Maconi G.
        • Carsana L.
        • Fociani P.
        • et al.
        Small bowel stenosis in Crohn's disease: clinical, biochemical and ultrasonographic evaluation of histological features.
        Alimentary Pharmacology and Therapeutics. 2003; 18: 749-756
        • Nylund K.
        • Jirik R.
        • Mezl M.
        • et al.
        Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn's disease.
        Ultrasound in Medicine and Biology. 2013; 39: 1197-1206
        • Ripollès T.
        • Rausell N.
        • Paredes J.M.
        • 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 and Colitis. 2013; 7: 120-128
        • Quaia E.
        Contrast-enhanced ultrasound of the small bowel in Crohn's disease.
        Abdominal Imaging. 2013; 38: 1005-1013
        • Kratzer W.
        • Von Tirpitz C.
        • Mason R.
        • et al.
        Contrast-enhanced power Doppler sonography of the intestinal wall in the differentiation of hypervascularized and hypovascularized intestinal obstructions in patients with Crohn's disease.
        Journal of Ultrasound in Medicine. 2002; 21: 149-157
        • Ophir J.
        • Céspedes I.
        • Ponnekanti H.
        • et al.
        Elastography: a quantitative method for imaging the elasticity of biological tissues.
        Ultrasonic Imaging. 1991; 13: 111-134
        • Kim K.
        • Johnson L.A.
        • Jia C.
        • et al.
        Noninvasive ultrasound elasticity imaging (UEI) of Crohn's disease: animal model.
        Ultrasound in Medicine and Biology. 2008; 34: 902-912
        • Stidham R.W.
        • Xu J.
        • Johnson L.A.
        • et al.
        Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn's disease.
        Gastroenterology. 2011; 141: 819-826
        • Baumgart D.C.
        • Müller H.P.
        • 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
        • Fraquelli M.
        • Branchi F.
        • Cribiù F.M.
        • et al.
        The role of ultrasound elasticity imaging in predicting ileal fibrosis in Crohn's disease patients.
        Inflammatory Bowel Diseases. 2015; 21: 2605-2612
        • Dillman J.R.
        • Stidham R.W.
        • Higgins P.D.
        • et al.
        Ultrasound shear wave elastography helps discriminate low-grade from high-grade bowel wall fibrosis in ex vivo human intestinal specimens.
        Journal of Ultrasound in Medicine. 2014; 33: 2115-2123
        • Dillman J.R.
        • Stidham R.W.
        • Higgins P.D.
        • 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
        • Palmeri M.L.
        • Nightingale K.R.
        Acoustic radiation force-based elasticity imaging methods.
        Interface Focus. 2011; 1: 553-564
        • Jess T.
        • Riis L.
        • Vind I.
        • et al.
        Changes in clinical characteristics, course, and prognosis of inflammatory bowel disease during the last 5 decades: a population-based study from Copenhagen, Denmark.
        Inflammatory Bowel Diseases. 2007; 13: 481-489
        • Allez M.
        • Lemann M.
        • Bonnet J.
        • et al.
        Long term outcome of patients with active Crohn's disease exhibiting extensive and deep ulcerations at colonoscopy.
        American Journal of Gastroenterology. 2002; 97: 947-953
        • Van Assche G.
        • Dignass A.
        • Panes J.
        • et al.
        The second European evidence-based Consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis.
        Journal of Crohn's and Colitis. 2010; 4: 7-27
        • Castiglione F.
        • De Sio I.
        • Cozzolino A.
        • et al.
        Bowel wall thickness at abdominal ultrasound and the one-year-risk of surgery in patients with Crohn's disease.
        American Journal of Gastroenterology. 2004; 99: 1977-1983
        • Maconi G.
        • Sampietro G.M.
        • Cristaldi M.
        • et al.
        Preoperative characteristics and postoperative behavior of bowel wall on risk of recurrence after conservative surgery in Crohn's disease: a prospective study.
        Annals of Surgery. 2001; 233: 345-352
        • Jauregui-Amezaga A.
        • Rimola J.
        • Ordás I.
        • et al.
        Value of endoscopy and MRI for predicting intestinal surgery in patients with Crohn's disease in the era of biologics.
        Gut. 2015; 64: 1397-1402
        • Frøslie K.F.
        • Jahnsen J.
        • Moum B.A.
        • et al.
        Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort.
        Gastroenterology. 2007; 133: 412-422
        • Solberg I.C.
        • Vatn M.H.
        • Høie O.
        • et al.
        Clinical course in Crohn's disease: results of a Norwegian population-based ten-year follow-up study.
        Clinical Gastroenterology and Hepatology. 2007; 5: 1430-1438
        • Baert F.
        • Moortgat L.
        • Van Assche G.
        • et al.
        Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease.
        Gastroenterology. 2010; 138: 463-468
        • Rutgeerts P.
        • Van Assche G.
        • Sandborn W.J.
        • et al.
        Adalimumab induces and maintains mucosal healing in patients with Crohn's disease: data from the EXTEND trial.
        Gastroenterology. 2012; 142: 1102-1111
        • Louis E.
        • Mary J.Y.
        • Vernier-Massouille G.
        • et al.
        Maintenance of remission among patients with Crohn's disease on antimetabolite therapy after infliximab therapy is stopped.
        Gastroenterology. 2012; 142: 63-70
        • Moreno N.
        • Ripollés T.
        • Paredes J.M.
        • et al.
        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.
        Journal of Crohn's and Colitis. 2014; 8: 1079-1087
        • Van Assche G.
        • Herrmann K.A.
        • Louis E.
        • et al.
        Effects of infliximab therapy on transmural lesions as assessed by magnetic resonance enteroclysis in patients with ileal Crohn's disease.
        Journal of Crohn's and Colitis. 2013; 7: 950-957
        • Tielbeek J.A.
        • Löwenberg M.
        • Bipat S.
        • et al.
        Serial magnetic resonance imaging for monitoring medical therapy effects in Crohn's disease.
        Inflammatory Bowel Diseases. 2013; 19: 1943-1950
        • Castiglione F.
        • Testa A.
        • Rea M.
        • et al.
        Transmural healing evaluated by bowel sonography in patients with Crohn's disease on maintenance treatment with biologics.
        Inflammatory Bowel Diseases. 2013; 19: 1928-1934
        • Lee E.C.
        • Papaioannou N.
        Recurrences following surgery for Crohn's disease.
        Clinics in Gastroenterology. 1980; 9: 419-438
        • Rutgeerts P.
        • Geboes K.
        • Vantrappen G.
        • et al.
        Predictability of the postoperative course of Crohn's disease.
        Gastroenterology. 1990; 99: 956-963
        • Orlando A.
        • Mocciaro F.
        • Renna S.
        • et al.
        Early post-operative endoscopic recurrence in Crohn's disease patients: data from an Italian Group for the study of inflammatory bowel disease (IG-IBD) study on a large prospective multicenter cohort.
        Journal of Crohn's and Colitis. 2014; 8: 1217-1221
        • Buisson A.
        • Chevaux J.B.
        • Allen P.B.
        • et al.
        Review article: the natural history of postoperative Crohn's disease recurrence.
        Alimentary Pharmacology and Therapeutics. 2012; 35: 625-633
        • Olaison G.
        • Smedh K.
        • Sjödahl R.
        Natural course of Crohn's disease after ileocolic resection: endoscopically visualised ileal ulcers preceding symptoms.
        Gut. 1992; 33: 331-335
        • 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: 489-494
        • Sailer J.
        • Peloschek P.
        • Reinisch W.
        • et al.
        Anastomotic recurrence of Crohn's disease after ileocolic resection: comparison of MR enteroclysis with endoscopy.
        European Radiology. 2008; 18: 2512-2521
        • Koilakou S.
        • Sailer J.
        • Peloschek P.
        • et al.
        Endoscopy and MR enteroclysis: equivalent tools in predicting clinical recurrence in patients with Crohn's disease after ileocolic resection.
        Inflammatory Bowel Diseases. 2010; 16: 198-203
        • Soyer P.
        • Boudiaf M.
        • Sirol M.
        • et al.
        Suspected anastomotic recurrence of Crohn disease after ileocolic resection: evaluation with CT enteroclysis.
        Radiology. 2010; 254: 755-764
        • Mao R.
        • Gao X.
        • Zhu Z.H.
        • et al.
        CT enterography in evaluating postoperative recurrence of Crohn's disease after ileocolic resection: complementary role to endoscopy.
        Inflammatory Bowel Diseases. 2013; 19: 977-982
        • Paparo F.
        • Revelli M.
        • Puppo C.
        • et al.
        Crohn's disease recurrence in patients with ileocolic anastomosis: value of computed tomography enterography with water enema.
        European Journal of Radiology. 2013; 82: e434-e440
        • Minordi L.M.
        • Vecchioli A.
        • Mirk P.
        • et al.
        CT enterography with polyethylene glycol solution vs CT enteroclysis in small bowel disease.
        British Journal of Radiology. 2011; 84: 112-119
        • Orlando A.
        • Modesto I.
        • Castiglione F.
        • et al.
        The role of calprotectin in predicting endoscopic post-surgical recurrence in asymptomatic Crohn's disease: a comparison with ultrasound.
        European Review for Medical and Pharmacological Sciences. 2006; 10: 17-22
        • Andreoli A.
        • Cerro P.
        • Falasco G.
        • et al.
        Role of ultrasonography in the diagnosis of postsurgical recurrence of Crohn's disease.
        American Journal of Gastroenterology. 1998; 93: 1117-1121
        • Pallotta N.
        • Giovannone M.
        • Pezzotti P.
        • et al.
        Ultrasonographic detection and assessment of the severity of Crohn's disease recurrence after ileal resection.
        BMC Gastroenterology. 2010; 10: 69
        • Onali S.
        • Calabrese E.
        • Petruzziello C.
        • et al.
        Endoscopic vs ultrasonographic findings related to Crohn's disease recurrence: a prospective longitudinal study at 3 years.
        Journal of Crohn's and Colitis. 2010; 4: 319-328
        • Rispo A.
        • Bucci L.
        • Pesce G.
        • et al.
        Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn's disease.
        Inflammatory Bowel Diseases. 2006; 12: 486-490
        • Castiglione F.
        • Bucci L.
        • Pesce G.
        • et al.
        Oral contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohn's disease.
        Inflammatory Bowel Diseases. 2008; 14: 1240-1245
        • Calabrese E.
        • Petruzziello C.
        • Onali S.
        • et al.
        Severity of postoperative recurrence in Crohn's disease: correlation between endoscopic and sonographic findings.
        Inflammatory Bowel Diseases. 2009; 15: 1635-1642
        • Paredes J.M.
        • Ripollés T.
        • Cortés X.
        • et al.
        Non-invasive diagnosis and grading of postsurgical endoscopic recurrence in Crohn's disease: usefulness of abdominal ultrasonography and 99mTc-hexamethylpropylene amineoxime-labelled leucocyte scintigraphy.
        Journal of Crohn's and Colitis. 2010; 4: 537-545
        • Parente F.
        • Sampietro G.M.
        • Molteni M.
        • et al.
        Behaviour of the bowel wall during the first year after surgery is a strong predictor of symptomatic recurrence of Crohn's disease: a prospective study.
        Alimentary Pharmacology and Therapeutics. 2004; 20: 959-968
        • Cammarota T.
        • Ribaldone D.G.
        • Resegotti A.
        • et al.
        Role of bowel ultrasound as a predictor of surgical recurrence of Crohn's disease.
        Scandinavian Journal of Gastroenterology. 2013; 48: 552-555
        • Cosnes J.
        • Cattan S.
        • Blain A.
        • et al.
        Long-term evolution of disease behavior of Crohn's disease.
        Inflammatory Bowel Diseases. 2002; 8: 244-250
        • Ziech M.L.
        • Lavini C.
        • Caan M.W.
        • et al.
        Dynamic contrast-enhanced MRI in patients with luminal Crohn's disease.
        European Journal of Radiology. 2012; 81: 3019-3027
        • Pariente B.
        • Cosnes J.
        • Danese S.
        • et al.
        Development of the Crohn's disease digestive damage score, the Lémann score.
        Inflammatory Bowel Diseases. 2011; 17: 1415-1422
        • Sharp J.T.
        • Wolfe F.
        • Mitchell D.M.
        • et al.
        The progression of erosion and joint space narrowing scores in rheumatoid arthritis during the first twenty-five years of disease.
        Arthritis and Rheumatism. 1991; 34: 660-668
        • Pariente B.
        • Peyrin-Biroulet L.
        • Cohen L.
        • et al.
        Gastroenterology review and perspective: the role of cross-sectional imaging in evaluating bowel damage in Crohn disease.
        American Journal of Roentgenology. 2011; 197: 42-49
        • Pariente B.
        • Mary J.Y.
        • Danese S.
        • et al.
        Development of the Lémann index to assess digestive tract damage in patients with Crohn's disease.
        Gastroenterology. 2015; 148: 52-63
        • Calabrese E.
        • Zorzi F.
        • Zuzzi S.
        • et al.
        Development of a numerical index quantitating small bowel damage as detected by ultrasonography in Crohn's disease.
        Journal of Crohn's and Colitis. 2012; 6: 852-860
        • Colli A.
        • Fraquelli M.
        • Casazza G.
        • et al.
        The architecture of diagnostic research: from bench to bedside – research guidelines using liver stiffness as an example.
        Hepatology. 2014; 60: 408-418