Abstract
Celiac disease is an autoimmune disorder that causes inflammation and destruction in the small intestine of genetically susceptible individuals following ingestion of gluten. Awareness of the disease has increased; however, it remains a challenge to diagnose. This review summarizes the intestinal and extraintestinal cross-sectional imaging findings of celiac disease. Small intestine fold abnormalities are the most specific imaging findings for celiac disease, whereas most other imaging findings reflect a more generalized pattern seen with malabsorptive processes. Familiarity with the imaging pattern may allow the radiologist to suggest the diagnosis in patients with atypical presentations in whom it is not clinically suspected. Earlier detection allows earlier treatment initiation and may prevent significant morbidity and mortality that can occur with delayed diagnosis. Refractory celiac disease carries the greatest risk of mortality due to associated complications, including cavitating mesenteric lymph node syndrome, ulcerative jejunoileitis, enteropathy-associated T cell lymphoma, and adenocarcinoma, all of which are described and illustrated. Radiologic and endoscopic investigations are complimentary modalities in the setting of complicated celiac disease.
Similar content being viewed by others
References
Green PH, Cellier C (2007) Celiac disease. N Engl J Med 357(17):1731–1743
Guandalini S, Assiri A (2014) Celiac disease: a review. JAMA Pediatr 168(3):272–278
Rubesin SE, et al. (1989) Adult celiac disease and its complications. Radiographics 9(6):1045–1066
Rubesin SE, Rubin RA, Herlinger H (1992) Small bowel malabsorption: clinical and radiologic perspectives. How we see it. Radiology 184(2):297–305
Paulsen SR, Huprich JE, Fletcher JG, et al. (2006) CT enterography as a diagnostic tool in evaluating small bowel disorders: review of clinical experience with over 700 cases. Radiographics 26(3):641–657, discussion 657–662
Oberhuber G, Granditsch G, Vogelsang H (1999) The histopathology of coeliac disease: time for a standardized report scheme for pathologists. Eur J Gastroenterol Hepatol 11(10):1185–1194
Shmidt E, Smyrk TC, Boswell CL, Enders FT, Oxentenko AS (2014) Increasing duodenal intraepithelial lymphocytosis found at upper endoscopy: time trends and associations. Gastrointest Endosc 80(1):105–111
Rubio-Tapia A, Hill ID, Kelly CP, Calderwood AH, Murray JA (2013) ACG clinical guidelines: diagnosis and management of celiac disease. Am J Gastroenterol 108(5):656–676 (quiz 677)
Lebwohl B, Rubio-Tapia A, Assiri A, Newland C, Guandalini S (2012) Diagnosis of celiac disease. Gastrointest Endosc Clin N Am 22(4):661–677
McGowan KE, Lyon ME, Butzner JD (2008) Celiac disease and IgA deficiency: complications of serological testing approaches encountered in the clinic. Clin Chem 54(7):1203–1209
Rubio-Tapia A, Rahim MW, See JA, et al. (2010) Mucosal recovery and mortality in adults with celiac disease after treatment with a gluten-free diet. Am J Gastroenterol 105(6):1412–1420
Hadithi M, Von Blomberg BME, Crusius JBA, et al. (2007) Accuracy of serologic tests and HLA-DQ typing for diagnosing celiac disease. Ann Intern Med 147(5):294–302
Kaukinen K, Partanen J, Mäki M, Collin P (2002) HLA-DQ typing in the diagnosis of celiac disease. Am J Gastroenterol 97(3):695–699
Megiorni F, Pizzuti A (2012) HLA-DQA1 and HLA-DQB1 in Celiac disease predisposition: practical implications of the HLA molecular typing. J Biomed Sci 19:88
Sollid LM, Thorsby E (1990) The primary association of celiac disease to a given HLA-DQ alpha/beta heterodimer explains the divergent HLA-DR associations observed in various Caucasian populations. Tissue Antigens 36(3):136–137
Scholz FJ, Behr SC, Scheirey CD (2007) Intramural fat in the duodenum and proximal small intestine in patients with celiac disease. AJR Am J Roentgenol 189(4):786–790
Van Weyenberg SJ, Mulder CJ, Van Waesberghe JH (2015) Small bowel imaging in celiac disease. Dig Dis 33(2):252–259
Tomei E, Diacinti D, Marini M, et al. (2005) Abdominal CT findings may suggest coeliac disease. Dig Liver Dis 37(6):402–406
Jones B, Bayless TM, Hamilton SR, Yardley JH (1984) “Bubbly” duodenal bulb in celiac disease: radiologic-pathologic correlation. AJR Am J Roentgenol 142(1):119–122
Schweiger GD, Murray JA (1998) Postbulbar duodenal ulceration and stenosis associated with celiac disease. Abdom Imaging 23(4):347–349
Jones B, Fishman EK, Hamilton SR, et al. (1986) Submucosal accumulation of fat in inflammatory bowel disease: CT/pathologic correlation. J Comput Assist Tomogr 10(5):759–763
Barlow JM, Johnson CD, Stephens DH (1996) Celiac disease: how common is jejunoileal fold pattern reversal found at small-bowel follow-through? AJR. Am J Roentgenol 166(3):575–577
Tomei E, Marini M, Messineo D, et al. (2000) Computed tomography of the small bowel in adult celiac disease: the jejunoileal fold pattern reversal. Eur Radiol 10(1):119–122
Bova JG, et al. (1985) Adaptation of the ileum in nontropical sprue: reversal of the jejunoileal fold pattern. AJR Am J Roentgenol 144(2):299–302
Herlinger H, Maglinte DD (1986) Jejunal fold separation in adult celiac disease: relevance of enteroclysis. Radiology 158(3):605–611
Soyer P, Boudiaf M, Dray X, et al. (2009) CT enteroclysis features of uncomplicated celiac disease: retrospective analysis of 44 patients. Radiology 253(2):416–424
Tomei E, Semelka RC, Braga L, et al. (2006) Adult celiac disease: what is the role of MRI? J Magn Reson Imaging 24(3):625–629
Eid M, Abougabal A, Zeid A (2013) Celiac disease: do not miss that diagnosis!. Egypt J Radiol Nucl Med 44(4):727–735
Scholz FJ, Afnan J, Behr SC (2011) CT findings in adult celiac disease. Radiographics 31(4):977–992
Marinis A, Yiallourou A, Samanides L, et al. (2009) Intussusception of the bowel in adults: a review. World J Gastroenterol 15(4):407–411
Briggs JH, McKean D, Palmer JS, Bungay H (2014) Transient small bowel intussusception in adults: an overlooked feature of coeliac disease. BMJ Case Reports: e203156.
Cohen MD, Lintott DJ (1978) Transient small bowel intussusception in adult coeliac disease. Clin Radiol 29(5):529–534
Gonda TA, Cheng J, Lewis SK, Rubin M, Green PH (2010) Association of intussusception and celiac disease in adults. Dig Dis Sci 55(10):2899–2903
Tursi A, Brandimarte G, Giorgetti G (2003) High prevalence of small intestinal bacterial overgrowth in celiac patients with persistence of gastrointestinal symptoms after gluten withdrawal. Am J Gastroenterol 98(4):839–843
Mallant M, Hadithi M, Al-Toma AB, et al. (2007) Abdominal computed tomography in refractory coeliac disease and enteropathy associated T-cell lymphoma. World J Gastroenterol 13(11):1696–1700
Al-Attar W, Majeed S, Shubbar A (2005) Superior mesenteric artery blood flow in celiac disease “Estimation with Doppler Ultrasound”. IJGE 1:38–43
Alvarez D, Vazquez H, Bai JC, et al. (1993) Superior mesenteric artery blood flow in celiac disease. Dig Dis Sci 38(7):1175–1182
Arienti V, Califano C, Brusco G, et al. (1996) Doppler ultrasonographic evaluation of splanchnic blood flow in coeliac disease. Gut 39(3):369–373
Rettenbacher T, Hollerweger A, Macheiner P, et al. (1999) Adult celiac disease: US signs. Radiology 211(2):389–394
Gustafson T, Sjolund K, Berg NO (1982) Intestinal circulation in coeliac disease: an angiographic study. Scand J Gastroenterol 17(7):881–885
Van Weyenberg SJ, Meijerink MR, Jacobs MA, et al. (2011) MR enteroclysis in refractory celiac disease: proposal and validation of a severity scoring system. Radiology 259(1):151–161
Lohan DG, Alhajeri AN, Cronin CG, Roche CJ, Murphy JM (2008) MR enterography of small-bowel lymphoma: potential for suggestion of histologic subtype and the presence of underlying celiac disease. AJR Am J Roentgenol 190(2):287–293
Branchi F, Locatelli M, Tomba C, et al. (2016) Enteroscopy and radiology for the management of celiac disease complications: time for a pragmatic roadmap. Dig Liver Dis 48(6):578–586
Abdulkarim AS, Burgart L, See J, Murray JA (2002) Etiology of nonresponsive celiac disease: results of a systematic approach. Am J Gastroenterol 97(8):2016–2021
Biagi F, Corazza GR (2001) Defining gluten refractory enteropathy. Eur J Gastroenterol Hepatol 13(5):561–565
Cellier C, Delabesse E, Helmer C, et al. (2000) Refractory sprue, coeliac disease, and enteropathy-associated T-cell lymphoma. Fr Coeliac Dis Study Group Lancet 356(9225):203–208
Al-toma A, Verbeek WH, Mulder CJ (2007) The management of complicated celiac disease. Dig Dis 25(3):230–236
Rubio-Tapia A, Kelly DG, Lahr BD, et al. (2009) Clinical staging and survival in refractory celiac disease: a single center experience. Gastroenterology 136(1):99–107 (quiz 352–353)
Holmes GK, Prior P, Lane MR, Pope D, Allan RN (1989) Malignancy in coeliac disease–effect of a gluten free diet. Gut 30(3):333–338
Malamut G, Afchain P, Verkarre V, et al. (2009) Presentation and long-term follow-up of refractory celiac disease: comparison of type I with type II. Gastroenterology 136(1):81–90
Elli L, Contiero P, Tagliabue G, Tomba C, Bardella MT (2012) Risk of intestinal lymphoma in undiagnosed coeliac disease: results from a registered population with different coeliac disease prevalence. Dig Liver Dis 44(9):743–747
Freeman HJ (2004) Lymphoproliferative and intestinal malignancies in 214 patients with biopsy-defined celiac disease. J Clin Gastroenterol 38(5):429–434
Smedby KE, Åkerman M, Hildebrand H, et al. (2005) Malignant lymphomas in coeliac disease: evidence of increased risks for lymphoma types other than enteropathy-type T cell lymphoma. Gut 54(1):54–59
Buckley O, Brien JO, Ward E, et al. (2008) The imaging of coeliac disease and its complications. Eur J Radiol 65(3):483–490
Van Weyenberg SJB, et al. (2008) Double balloon endoscopy in celiac disease. Tech Gastrointest Endosc 10(2):87–93
Meijer JW, Mulder CJJ, Goerres MG, Boot H, Schweizer JJ (2004) Coeliac disease and (extra)intestinal T-cell lymphomas: definition, diagnosis and treatment. Scand J Gastroenterol Suppl 39(241):78–84
Brousse N, Meijer JW (2005) Malignant complications of coeliac disease. Best Pract Res Clin Gastroenterol 19(3):401–412
Freeman HJ, Chiu BK (1986) Small bowel malignant lymphoma complicating celiac sprue and the mesenteric lymph node cavitation syndrome. Gastroenterology 90(6):2008–2012
van de Water JM, Nijeboer P, de Baaij LR, et al. (2015) Surgery in (pre)malignant celiac disease. World J Gastroenterol 21(43):12403–12409
Masselli G, Gualdi G (2010) Evaluation of small bowel tumors: MR enteroclysis. Abdom Imaging 35(1):23–30
Swinson CM, Coles EC, Slavin G, Booth CC (1983) Coeliac disease and malignancy. Lancet 1(8316):111–115
Freeman HJ (2009) Malignancy in adult celiac disease. World J Gastroenterol 15(13):1581–1583
Freeman HJ (2010) Mesenteric lymph node cavitation syndrome. World J Gastroenterol 16(24):2991–2993
Reddy D, Salomon C, Demos TC, Cosar E (2002) Mesenteric lymph node cavitation in celiac disease. AJR Am J Roentgenol 178(1):247
Huppert BJ, Farrell MA, Kawashima A, Murray JA (2004) Diagnosis of cavitating mesenteric lymph node syndrome in celiac disease using MRI. AJR Am J Roentgenol 183(5):1375–1377
Yamamoto H, Sekine Y, Sato Y, et al. (2001) Total enteroscopy with a nonsurgical steerable double-balloon method. Gastrointest Endosc 53(2):216–220
Rondonotti E, Spada C, Cave D (2007) Video capsule enteroscopy in the diagnosis of celiac disease: a multicenter study. Am J Gastroenterol 102(8):1624–1631
Rondonotti E, Villa F, Saladino V, de Franchis R (2009) Enteroscopy in the diagnosis and management of celiac disease. Gastrointest Endosc Clin N Am 19(3):445–460
Valitutti F, Di Nardo G, Barbato M, et al. (2014) Mapping histologic patchiness of celiac disease by push enteroscopy. Gastrointest Endosc 79(1):95–100
Heine GD, Hadithi M, Groenen MJM, et al. (2006) Double-balloon enteroscopy: indications, diagnostic yield, and complications in a series of 275 patients with suspected small-bowel disease. Endoscopy 38(1):42–48
Daum S, et al. (2007) Capsule endoscopy in refractory celiac disease. Endoscopy 39(5):455–458
Muhammad A, Pitchumoni CS (2008) Newly detected celiac disease by wireless capsule endoscopy in older adults with iron deficiency anemia. J Clin Gastroenterol 42(9):980–983
Atlas DS, Rubio-Tapia A, Van Dyke CT, Lahr BD, Murray JA (2011) Capsule endoscopy in nonresponsive celiac disease. Gastrointest Endosc 74(6):1315–1322
Hara AK, Leighton JA, Sharma VK, Heigh RI, Fleischer DE (2005) Imaging of small bowel disease: comparison of capsule endoscopy, standard endoscopy, barium examination, and CT. Radiographics 25(3):697–711, discussion 711–718
Hadithi M, Mallant M, Oudejans J, et al. (2006) 18F-FDG PET versus CT for the detection of enteropathy-associated T-cell lymphoma in refractory celiac disease. J Nucl Med 47(10):1622–1627
Fuchs V, Kurppa K, Huhtala H, et al. (2014) Factors associated with long diagnostic delay in celiac disease. Scand J Gastroenterol 49(11):1304–1310
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
No funding was received for this study.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Statement of informed consent was not applicable since the manuscript does not contain any patient data.
Rights and permissions
About this article
Cite this article
Sheedy, S.P., Barlow, J.M., Fletcher, J.G. et al. Beyond moulage sign and TTG levels: the role of cross-sectional imaging in celiac sprue. Abdom Radiol 42, 361–388 (2017). https://doi.org/10.1007/s00261-016-1006-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00261-016-1006-2