Advertisement

Ultrasound

  • Nadia PallottaEmail author
  • Enrico S. CorazziariEmail author
Chapter

Abstract

The management of patients with inflammatory bowel disease (IBD) requires evaluation with objective tools, both at the time of diagnosis and throughout the course of the disease, to determine the location, extension, activity and severity of inflammatory lesions, as well as, the development of complications. Bowel ultrasound—which is well accepted by patients, non-invasive inexpensive and widely accessible—has been successfully employed as the imaging technique of choice in screening patients with clinically suspected IBD as well as in the follow-up of patients with known Crohn’s disease to assess the site and extent of the lesions, early detection of intraabdominal complications, and recurrence in those submitted to resective surgery. Despite several attempts to correlate ultrasound findings with clinical and biochemical activity, there are as yet no convincing data on the usefulness of ultrasound in assessing the activity of Crohn’s disease.

Keywords

Transabdominal ultrasound (TUS) Small intestine contrast ultrasonography (SICUS) Crohn’s disease Ulcerative colitis CD abdominal complication CD recurrence lesions Oral contrast ultrasonography CEUS Bowel doppler ultrasound 

Supplementary material

Video 2.1

SICUS video showing normal jejunal loops. The oral contrast distending the intestinal lumen allows to visualize and assess the thickness of intestinal wall and the presence and distribution of intestinal folds. (MP4 5,172 kb)

Video 2.2

SICUS video showing a pathological CD ileal tract. (MP4 1,871 kb)

Video 2.3

SICUS video showing a pathological CD ileal tract with reduced lumen diameter. The oral contrast distending the intestinal lumen allows to measure lumen diameter and motor activity of intestinal wall. (MP4 5,210 kb)

Video 2.4

SICUS video showing several pathological CD ileal tracts. Note the hypoechoic duct-like shaped images arising from the thickened intestinal wall through a wrapping mesentery and through the adjacent pathological tract. (MP4 7,339 kb)

References

  1. 1.
    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. J Crohns Colitis. 2010;4:7–27.PubMedCrossRefGoogle Scholar
  2. 2.
    Goldberg HI, Caruthers SB, Nelson JA, Singleton JW. Radiographic findings of the national cooperative Crohn’s disease study. Gastroenterology. 1979;77:925–37.PubMedGoogle Scholar
  3. 3.
    Podolsky DK. Inflammatory bowel disese. N Engl J Med. 1991;325:928–37.PubMedCrossRefGoogle Scholar
  4. 4.
    Loftus EV, Schoenfeld P, Sandborn WJ. The epidemiology and natural history of Crohn’s disease in population-based patient cohorts from North America: a systematic review. Aliment Pharmacol Ther. 2002;16:51–60.PubMedCrossRefGoogle Scholar
  5. 5.
    Sauer CG, Kugathasan S. Pediatric inflammatory bowel disease: highlighting pediatric differences in IBD. Med Clin North Am. 2010;94:35–52.PubMedCrossRefGoogle Scholar
  6. 6.
    Ott DJ, Chen VM, Gelfand DW, Van Swearingen F, Munitz HA. Detailed per-oral small bowel examination vs entereroclysis. Radiology. 1985;155:29–34.PubMedCrossRefGoogle Scholar
  7. 7.
    Toms AP, Barltrop A, Freeman AH. A prospective randomised study comparing enteroclysis with small bowel follow-trough examinations in 244 patients. Eur Radiol. 2001;11:1155–60.PubMedCrossRefGoogle Scholar
  8. 8.
    Hara AK, Leighton JA, Sharma VK, Fleischer DE. Small bowel: preliminary comparison of capsule endoscopy with barium study and CT. Radiology. 2004;230:260–65.PubMedCrossRefGoogle Scholar
  9. 9.
    Agency for Healthcare Research and Quality. ACR appropriateness criteria: Crohn disease. Available from: http://guideline.gov/content.aspx?id=35137. Accessed 16 Apr 2013.
  10. 10.
    Kroeker KI, Lam S, Birchall I, Fedorak RN. Patients with IBD are exposed to high levels of ionizing radiation through CT scan diagnostic imaging: a five-year study. J Clin Gastroenterol. 2011;45:34–9.PubMedCrossRefGoogle Scholar
  11. 11.
    Sauer CG. Radiation exposure in children with inflammatory bowel disease. Curr Opin Pediatr. 2012;24:621–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Desmond AN, O’Regan K, Curran C, et al. Crohn’s disease: factors associated with exposure to high levels of diagnostic radiation. Gut. 2008;57:1524–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Joanna M, Peloquin JM, Pardi DS, et al. Diagnostic ionizing radiation exposure in a population-based cohort of patients with inflammatory bowel disease. Am J Gastroenterol. 2008;103:2015–22.CrossRefGoogle Scholar
  14. 14.
    Valette PJ, Rioux M, Pilleul F, et al. Ultrasonography of chronic inflammatory bowel diseases. Eur Radiol. 2001;11:1859–66.PubMedCrossRefGoogle Scholar
  15. 15.
    Maconi G, Radice E, Greco S, Bianchi PG. Bowel ultrasound in Crohn’s disease. Best Pract Res Clin Gastroenterol. 2006;20:93–112.PubMedCrossRefGoogle Scholar
  16. 16.
    Di Nardo G, Aloi M, Oliva S, Civitelli F, Casciani E, Cucchiara S. Investigation of small bowel in pediatric Crohn’s disease. Inflamm Bowel Dis. 2012;18:1760–76.PubMedCrossRefGoogle Scholar
  17. 17.
    Pallotta N, Tomei E, Viscido A, Calabrese E, Marcheggiano A, Caprilli R, et al. Small intestine contrast ultrasonography: an alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis. 2005;11:146–53.PubMedCrossRefGoogle Scholar
  18. 18.
    Pallotta N, Baccini F, Corazziari E. Ultrasonography of the small bowel after oral administration of anechoich contrast solution. Lancet. 1999;353:985–6.PubMedCrossRefGoogle Scholar
  19. 19.
    Pallotta N, Baccini F, Corazziari E. Contrast ultrasonography of the normal small bowel. Ultrasound Med Biol. 1999;25:1335–40.PubMedCrossRefGoogle Scholar
  20. 20.
    Pallotta N, Baccini F, Corazziari E. Small intestine contrast ultrasonography (SICUS) in the diagnosis of small intestine lesions. Ultrasound Med Biol. 2001;27:335–41.PubMedCrossRefGoogle Scholar
  21. 21.
    Di Sabatino A, Fulle I, Ciccocioppo R, et al. Doppler enhancement after intravenous levovist injection in Crohn’s disease. Inflamm Bowel Dis. 2002;8:251–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Schlottmann K, Kratzer W, Scholmerich J. Doppler ultrasound and intravenous contrast agents in gastrointestinal tract disorders: current role and future implications. Eur J Gastroenterol Hepatol. 2005;17:263–75.PubMedCrossRefGoogle Scholar
  23. 23.
    Drews BH, Barth TF, Hanle MM, et al. Comparison of sonographically measured bowel wall vascularity, histology, and disease activity in Crohn’s disease. Eur Radiol. 2009;19:1379–86.PubMedCrossRefGoogle Scholar
  24. 24.
    Nylund K, Hausken T, Gilja OH. Ultrasound and inflammatory bowel disease. Ultrasound Q. 2010;26:3–15.PubMedCrossRefGoogle Scholar
  25. 25.
    Holt S, Samuel E. Grey scale ultrasound in Crohn’s disease. Gut. 1979;20:590–5.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Parente F, Greco S, Molteni M, Anderloni A, Maconi G, Bianchi PG. Modern imaging of Crohn’s disease using bowel ultrasound. Inflamm Bowel Dis. 2004;10:452–61.PubMedCrossRefGoogle Scholar
  27. 27.
    Fraquelli M, Colli A, Casazza G, Paggi S, Colucci A, Massironi S, et al. Role of US in detection of Crohn disease: meta-analysis. Radiology. 2005;236:95–101.PubMedCrossRefGoogle Scholar
  28. 28.
    Pallotta N, Civitelli F, Di Nardo G, Vincoli G, Aloi M, Viola F, Capocaccia P, Corazziari E, Cucchiara S. Small intestine contrast ultrasonography in pediatric Crohn’s disease. J Pediatr. 2013;163:778–84.PubMedCrossRefGoogle Scholar
  29. 29.
    Pallotta N, Vincoli G, Montesani C, Chirletti P, Pronio A, Caronna R, Ciccantelli B, Romeo E, Marcheggiano A, Corazziari E. Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in Crohn’s disease: a prospective comparative study versus intraoperative findings. Inflamm Bowel Dis. 2012;18:74–84.PubMedCrossRefGoogle Scholar
  30. 30.
    Cittadini G, Giasotto V, Garlaschi G, de Cicco E, Gallo A, Cittadini G. Transabdominal ultrasonography of the small bowel after oral administration of a non-absorbable anechoic solution: comparison with barium enteroclysis. Clin Radiol. 2001;56:225–30.PubMedCrossRefGoogle Scholar
  31. 31.
    Folvik G, Bjerke-Larssen T, Odegaard S, Hausken T, Gilja H, Berstad A. Hydrosonography of the small intestine: comparison with radiologic barium study. Scand J Gastroenterol. 1999;34:1247–52.PubMedCrossRefGoogle Scholar
  32. 32.
    Parente F, Greco S, Molteni M, Anderloni A, Sampietro GM, Danelli PG, et al. 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;53:1652–7.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Parente F, Greco S, Molteni M, Cucino C, Maconi G, Sampietro GM, Danelli PG, Cristalli M, Bianco R, Gallus S, Bianchi PG. Role of the early ultrasound in detecting inflammatory intestinal disorders and identifying their anatomical location within the bowel. Aliment Pharmacol Ther. 2003;18:1009–16.PubMedCrossRefGoogle Scholar
  34. 34.
    Limberg B. Hydrocolonic ultrasonography. N Engl J Med. 1995;332:1581.PubMedCrossRefGoogle Scholar
  35. 35.
    Parente F, Maconi G, Bollani S, Anderloni A, Sampietro G, Cristaldi M, Franceschelli N, Bianco R, Taschieri AM, Bianchi PG. 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;50:490–5.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Pedersen Hojlund B, Gronvall S, Dorph S, Fahrenkrug L, Holm HH, Binder V. The value of dynamic ultrasound scanning in Crohn’s disease. Scand J Gastroenterol. 1986;21:969–72.CrossRefGoogle Scholar
  37. 37.
    Lim Hoon J, Tae Ko Y, Lee Ho D, Lim Won J, Kim Hoon T. Sonography of inflammatory bowel disease: findings and value in differential diagnosis. Am J Roentgenol. 1994;163:343–47.CrossRefGoogle Scholar
  38. 38.
    Sostegni R, Daperno M, Scaglione N et al. Crohn’s disease: monitoring disease activity. Aliment Pharmacol Ther 2003;17 (Suppl 2): 11–17.Google Scholar
  39. 39.
    Yoshida EM. The Crohn’s disease activity index, its derivatives and the inflammatory bowel disease questionnaire: a review of instruments to assess Crohn’s disease. Can J Gastroenterol. 1999;13:65–73.PubMedGoogle Scholar
  40. 40.
    Maconi G, Parente F, Bollani S, Cesana B, Bianchi PG. 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;91:1604–9.PubMedGoogle Scholar
  41. 41.
    Futagami Y, Haruma K, Hata J, Fujimura J, Tani H, Okamoto E, et al. Development and validation of an ultrasonographic activity index of Crohn’s disease. Eur J Gastroenterol Hepatol. 1999;11:1007–12.PubMedCrossRefGoogle Scholar
  42. 42.
    Martinez MJ, Ripolles T, Paredes JM, Blanc E, Marti-Bonmati L. Assessment of the extension and the inflammatory activity in Crohn’s disease: comparison of ultrasound and MRI. Abdom Imaging. 2009;34:141–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Hatoum OA, Miura H, Binion DG. The vascular contribution in the pathogenesis of inflammatory bowel disease. Am J Physiol Heart Circ Physiol. 2003;285:H1791–6.PubMedGoogle Scholar
  44. 44.
    Ripolles T, Martinez MJ, Paredes JM, et al. Crohn disease: correlation of findings at contrast-enhanced US with severity at endoscopy. Radiology. 2009;253:241–8.PubMedCrossRefGoogle Scholar
  45. 45.
    Girlich C, Jung EM, Iesalnieks I, et al. Quantitative assessment of bowel wall vascularisation in Crohn’s disease with contrast-enhanced ultrasound and perfusion analysis. Clin Hemorheol Microcirc. 2009;43:141–8.PubMedGoogle Scholar
  46. 46.
    Kratzer W, Schmidt SA, Mittrach C, et al. Contrast-enhanced wideband harmonic imaging ultrasound (SonoVue): a new technique for quantifying bowel wall vascularity in Crohn’s disease. Scand J Gastroenterol. 2005;40:985–91.PubMedCrossRefGoogle Scholar
  47. 47.
    Quaia E, Migaleddu V, Baratella E, et al. 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. 2009;69:438–44.PubMedCrossRefGoogle Scholar
  48. 48.
    Migaleddu V, Quaia E, Scanu D, et al. Inflammatory activity in Crohn’s disease: CE-US. Abdom Imaging. 2011;36:142–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Wong DD, Forbes GM, Zelesco M, Mason R, Pawlik J, Mendelson RM. Crohn’s disease activity: quantitative contrast-enhanced ultrasound assessment. Abdom Imaging. 2012;37:369–76.PubMedCrossRefGoogle Scholar
  50. 50.
    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. Am J Gastroenterol. 2003;98:1545–55.PubMedCrossRefGoogle Scholar
  51. 51.
    Chiorean MV, Sandrasegaran K, Saxena R, et al. Correlation of CT enteroclysis with surgical pathology in Crohn’s disease. Am J Gastroenterol. 2007;102:2541–50.PubMedCrossRefGoogle Scholar
  52. 52.
    Maglinte DD, Siegelman ES, Kelvin FM. MR enteroclysis: the future of small-bowel imaging? Radiology. 2000;215:639–41.PubMedCrossRefGoogle Scholar
  53. 53.
    Roses RE, Rombeau JL. Recent trends in the surgical management of inflammatory bowel disease. World J Gastroenterol. 2008;21:408–11.CrossRefGoogle Scholar
  54. 54.
    Cosnes J, Cattan S, Blain A, Beaugerie L, Carbonnel F, Parc R, Gendre JP. Long-term evolution of disease behavior of Crohn’s disease. Inflamm Bowel Dis. 2002;8:244–50.PubMedCrossRefGoogle Scholar
  55. 55.
    Otterson MF, Lundeen SJ, Spinelli KS, et al. Radiographic underestimation of small bowel stricturing Crohn’s disease: a comparison with surgical findings. Surgery. 2004;136:854–60.PubMedCrossRefGoogle Scholar
  56. 56.
    Maconi G, Bollani S, Bianchi PG. US detection of intestinal complications in Crohn’s disease. Dig Dis Sci. 1996;41:1643–8.PubMedCrossRefGoogle Scholar
  57. 57.
    Gasche C, Moser G, Turetschek K, et al. Transabdominal bowel sonography for detection of intestinal complication in Crohn’s disease. Gut. 1999;44:112–7.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Maconi G, Carsana L, Fociani P, et al. Small bowel stenosis in Crohn’s disease: clinical, biochemical and US evaluation of histological features. Aliment Pharmacol Ther. 2003;18:749–56.PubMedCrossRefGoogle Scholar
  59. 59.
    Di Sabatino A, Ciccocioppo R, Armellini E, et al. Serum bFGF and VEGF correlate respectively with bowel wall thickness and intramural blood flow in Crohn’s disease. Inflamm Bowel Dis. 2004;10:573–7.PubMedCrossRefGoogle Scholar
  60. 60.
    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. J Ultrasound Med. 2002;21:149–57.PubMedGoogle Scholar
  61. 61.
    Migaleddu V, Scanu AM, Quaia E, Rocca PC, Dore MP, Scanu D, et al. Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn’s disease. Gastroenterology. 2009;137:43–52.PubMedCrossRefGoogle Scholar
  62. 62.
    Bruining DH, Siddiki HA, Fletcher JG, Tremaine WJ, Sandborn WJ, Loftus EV. Prevalence of penetrating disease and extraintestinal manifestations of Crohn’s disease detected with CT enterography. Inflamm Bowel Dis. 2008;14:1701–06.PubMedCrossRefGoogle Scholar
  63. 63.
    Michelassi F, Stella M, Balestracci T, et al. Incidence, diagnosis, and treatment of enteric and colorectal fistulae in patients with Crohn’s disease. Ann Surg. 1993;218:660–6.PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Maconi G, Sampietro GM, Russo A, et al. The vascularity of internal fistulae in Crohn’s disease: an in vivo power Doppler ultrasonography assessment. Gut. 2002;50:496–500.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Maconi G, Parente F, Bianchi PG. Hydrogen peroxide enhanced ultrasound-fistulography in the assessment of enterocutaneous fistulas complicating Crohn’s disease. Gut. 1999;45:874–8.PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Kohn A, Cerro P, Milite G, et al. Prospective evaluation of transabdominal bowel sonography in the diagnosis of intestinal obstruction in Crohn’s disease: comparison with plain abdominal film and small bowel enteroclysis. Inflamm Bowel Dis. 1999;5:153–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Sheehan AL, Warren BF, Gear MW, et al. Fat-wrapping in Crohn’s disease: pathological basis and relevance to surgical practice. Br J Surg. 1992;79:955–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Maconi G, Greco S, Duca P, et al. Prevalence and clinical significance of sonographic evidence of mesenteric fat alterations in Crohn’s disease. Inflamm Bowel Dis. 2008;14:1555–61.PubMedCrossRefGoogle Scholar
  69. 69.
    Rutgeerts P, Geboes K, Vantrappen G, Beyls J, Kerremans R, Hiele M. Predictability of the postoperative course of Crohn’s disease. Gastroenterology. 1990;99:956–63.PubMedGoogle Scholar
  70. 70.
    Olaison G, Smedh K, Sjodahl R. Natural course of Crohn’s disease after ileo-colic resection: endoscopically visualised ileal ulcers preceeding symptoms. Gut. 1992;33:331–5.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Cottone M, Orlando A, Viscido A, Calbrese E, Cammà C, Casa A. Review article: prevention of postsurgical relapse and recurrence in Crohn’s disease. Aliment Pharmacol Ther. 2003;17(2):38–42.PubMedCrossRefGoogle Scholar
  72. 72.
    Belsy J, Epstein O, Heresbach D. Systematic review:oral bowel preparation for colonoscopy. Aliment Pharmacol Ther. 2007;25:373–84.CrossRefGoogle Scholar
  73. 73.
    Patak MA, Froehlich JM, Weymarn C, Ritz MA, Zollikofer CL, Wentz KU. Non-invasive distension of the small bowel for magnetic resonance imaging. Lancet. 2001;258:987–8.CrossRefGoogle Scholar
  74. 74.
    Rispo A, Bucci L, Pesce G, Sabbatini F, De Palma GD, Grassia R, Compagna A, Testa A, Castiglione F. Bowel sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm Bowel Dis. 2006;12:486–90.PubMedCrossRefGoogle Scholar
  75. 75.
    Castiglione F, Bucci L, Pesce G, De Palma GD, Camera L, Cipolletta F, Testa A, Diaferia M, Rispo A. Oral Contrast-enhanced sonography for the diagnosis and grading of postsurgical recurrence of Crohn’s disease. Inflamm Bowel Dis. 2008;14:1240–45.PubMedCrossRefGoogle Scholar
  76. 76.
    Calabrese E, Petruzziello C, Onali S, Condino G, Zorzi F, Pallone F, Biancone L. Severity of postoperative recurrence in Crohn’s disease: correlation between endoscopic and sonographic findings. Inflamm Bowel Dis. 2009;30.Google Scholar
  77. 77.
    Pallotta N, Giovannone M, Pezzotti P, Gigliozzi A, Barberani F, Piacentino D, Hassan NA, Vincoli G, Tosoni M, Covotta A, Marcheggiano A, Di Camillo M, Corazziari E. Ultrasonographic detection and assessment of the severity of Crohn’s disease recurrence after ileal resection. BMC Gastroenterol. 2010;10:69.PubMedCentralPubMedCrossRefGoogle Scholar
  78. 78.
    Ordas I, Rimola J, Rodriguez S, Gallego M, Ricart E, Panes J. Imaging of the colon in inflammatory bowel disease: ready for prime time? Curr Drug Targets. 2012;13:1252–60.PubMedCrossRefGoogle Scholar
  79. 79.
    Parente F, Molteni M, Marino B, Colli A, Ardizzone S, Greco S, et al. Are colonoscopy and bowel ultrasound useful for assessing response to short-term therapy and predicting disease outcome of moderate-to-severe forms of ulcerative colitis? a prospective study. Am J Gastroenterol. 2010;105:1150–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Bremner AR, Griffiths M, Argent JD, Fairhurst JJ, Beattie RM. Sonographic evaluation of inflammatory bowel disease: a prospective, blinded, comparative study. Pediatr Radiol. 2006;36:947–53.PubMedCrossRefGoogle Scholar
  81. 81.
    Antonelli E, Giuliano V, Casella G, Villanacci V, Baldini V, Baldoni M. Ultrasonographic assessment of colonic wall in moderate-severe ulcerative colitis: comparison with endoscopic findings. Dig Liver Dis. 2011;43:703–6.PubMedCrossRefGoogle Scholar
  82. 82.
    Civitelli F, Di Nardo G, Oliva S, Nuti F, Ferrari F, Dilillo A,Viola F, Pallotta N, Cucchiara S, Aloi M. Ultrasonography of the colon in pediatric ulcerative colitis: a prospective, blind, comparative study with colonoscopy. J Pediatr 2014;165(1):78–84 e2.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Internal Medicine and Medical SpecialtiesAzienda Policlinico Umberto IRomeItaly

Personalised recommendations