Skip to main content
SpringerLink
Log in

Does contrast-enhanced computed tomography raise awareness in the diagnosis of the invisible side of celiac disease in adults?

  • Hollow Organ GI
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Purpose

This study aimed to evaluate the diagnosis and determine major and minor criteria of celiac disease (CD) with the malabsorption patterns (MABP) in the small intestine and colon on computed tomography (CT) and additional CT findings.

Methods

This retrospective study was conducted with 116 patients diagnosed with CD, 14 CD patients recovering with treatment, and 35 control patients with non-CD. All patients had CT examinations and histopathological diagnoses. The sensitivity, specificity, PPV, NPV, and accuracy values of each CT finding defined in the literature were statistically evaluated. According to the patient and control groups, the numerical values of the findings and the sensitivity and specificity values were measured according to this cut-off value. The distribution of CT findings according to pathological Marsh data was evaluated in CD patients.

Results

Sensitivity and specificity were found to be higher in small bowel MABP findings, mesenteric hypervascularity, and increased SMV/aorta diameter. There was a numerically significant difference in MDCT findings between the control and pathological Marsh groups. In the ROC analysis performed in terms of the total numerical values of each MDCT finding observed between the groups, it was found that there were more than 7 MDCT findings, 100% sensitivity, and 92% specificity. The presence of four major and three minor criteria or three major and four minor criteria were considered significant.

Conclusions

Being aware of CT findings below the iceberg that may suggest CD in abdominal CT examinations performed in patients with atypical clinical and malabsorption findings or other nonspecific findings may prevent diagnostic delay and unnecessary procedures.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Singh P, Arora A, Strand TA, Leffler DA, Catassi C, Green PH, et al. (2018) Global Prevalence of Celiac Disease: Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol.16(6):823–36 e2. https://doi.org/10.1016/j.cgh.2017.06.037

  2. Shah S, Akbari M, Vanga R, Kelly CP, Hansen J, Theethira T, et al. (2014) Patient perception of treatment burden is high in celiac disease compared with other common conditions. Am J Gastroenterol.109(9):1304-11. https://doi.org/https://doi.org/10.1038/ajg.2014.29

    Article  PubMed  PubMed Central  Google Scholar 

  3. Missbach B, Schwingshackl L, Billmann A, Mystek A, Hickelsberger M, Bauer G, et al. (2015) Gluten-free food database: the nutritional quality and cost of packaged gluten-free foods. PeerJ.3:e1337. https://doi.org/https://doi.org/10.7717/peerj.1337

    Article  PubMed  PubMed Central  Google Scholar 

  4. Pourhoseingholi MA, Rostami-Nejad M, Barzegar F, Rostami K, Volta U, Sadeghi A, et al. (2017) Economic burden made celiac disease an expensive and challenging condition for Iranian patients. Gastroenterol Hepatol Bed Bench.10(4):258-62. PMID: 29379589

    PubMed  PubMed Central  Google Scholar 

  5. Koerner TB, Cleroux C, Poirier C, Cantin I, La Vieille S, Hayward S, et al. (2013) Gluten contamination of naturally gluten-free flours and starches used by Canadians with celiac disease. Food Addit Contam Part A Chem Anal Control Expo Risk Assess.30(12):2017-21. https://doi.org/https://doi.org/10.1080/19440049.2013.840744

    Article  CAS  PubMed  Google Scholar 

  6. Farage P, de Medeiros Nobrega YK, Pratesi R, Gandolfi L, Assuncao P, Zandonadi RP (2017) Gluten contamination in gluten-free bakery products: a risk for coeliac disease patients. Public Health Nutr.20(3):413-6. https://doi.org/https://doi.org/10.1017/S1368980016002433

    Article  PubMed  Google Scholar 

  7. Ciacci C, Zingone F (2015) The Perceived Social Burden in Celiac Disease. Diseases.3(2):102-10. https://doi.org/https://doi.org/10.3390/diseases3020102

    Article  PubMed  PubMed Central  Google Scholar 

  8. King JA, Kaplan GG, Godley J (2019) Experiences of coeliac disease in a changing gluten-free landscape. J Hum Nutr Diet.32(1):72-9. https://doi.org/https://doi.org/10.1111/jhn.12597

    Article  CAS  PubMed  Google Scholar 

  9. Ludvigsson JF (2012) Mortality and malignancy in celiac disease. Gastrointest Endosc Clin N Am.22(4):705-22. https://doi.org/https://doi.org/10.1016/j.giec.2012.07.005

    Article  PubMed  Google Scholar 

  10. Kochhar R, Jain K, Thapa BR, Rawal P, Khaliq A, Kochhar R, et al. (2012) Clinical presentation of celiac disease among pediatric compared to adolescent and adult patients. Indian J Gastroenterol.31(3):116-20. https://doi.org/https://doi.org/10.1007/s12664-012-0198-9

    Article  PubMed  Google Scholar 

  11. Kivela L, Kaukinen K, Lahdeaho ML, Huhtala H, Ashorn M, Ruuska T, et al. (2015) Presentation of Celiac Disease in Finnish Children Is No Longer Changing: A 50-Year Perspective. J Pediatr.167(5):1109–15 e1. https://doi.org/10.1016/j.jpeds.2015.07.057

  12. Dominguez Castro P, Harkin G, Hussey M, Christopher B, Kiat C, Liong Chin J, et al. (2017) Changes in Presentation of Celiac Disease in Ireland From the 1960s to 2015. Clin Gastroenterol Hepatol.15(6):864–71 e3. https://doi.org/10.1016/j.cgh.2016.11.018

  13. Parzanese I, Qehajaj D, Patrinicola F, Aralica M, Chiriva-Internati M, Stifter S, et al. (2017) Celiac disease: From pathophysiology to treatment. World J Gastrointest Pathophysiol.8(2):27-38. https://doi.org/https://doi.org/10.4291/wjgp.v8.i2.27

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sharma M, Singh P, Agnihotri A, Das P, Mishra A, Verma AK, et al. (2013) Celiac disease: a disease with varied manifestations in adults and adolescents. J Dig Dis.14(10):518-25. https://doi.org/https://doi.org/10.1111/1751-2980.12078

    Article  PubMed  Google Scholar 

  15. Rubio-Tapia A, Kyle RA, Kaplan EL, Johnson DR, Page W, Erdtmann F, et al. (2009) Increased prevalence and mortality in undiagnosed celiac disease. Gastroenterology.137(1):88-93. https://doi.org/https://doi.org/10.1053/j.gastro.2009.03.059

    Article  PubMed  Google Scholar 

  16. Ensari A, Marsh MN (2019) Diagnosing celiac disease: A critical overview. Turk J Gastroenterol.30(5):389-97. https://doi.org/https://doi.org/10.5152/tjg.2018.18635

    Article  PubMed  PubMed Central  Google Scholar 

  17. Goya C, Dundar I, Ozgokce M, Turkoglu S, Turko E, Ozkacmaz S, et al. (2021) Evaluation of celiac disease with uniphasic and multiphasic dynamic MDCT imaging. Abdom Radiol (NY).46(12):5564–73. https://doi.org/10.1007/s00261-021-03253-y

  18. Lomoschitz F, Schima W, Schober E, Turetschek K, Kaider A, Vogelsang H (2003) Enteroclysis in adult celiac disease: diagnostic value of specific radiographic features. Eur Radiol.13(4):890-6. https://doi.org/https://doi.org/10.1007/s00330-002-1455-6

    Article  CAS  PubMed  Google Scholar 

  19. Macari M, Megibow AJ, Balthazar EJ (2007) A pattern approach to the abnormal small bowel: observations at MDCT and CT enterography. AJR Am J Roentgenol.188(5):1344-55. https://doi.org/https://doi.org/10.2214/AJR.06.0712

    Article  PubMed  Google Scholar 

  20. Masselli G, Picarelli A, Di Tola M, Libanori V, Donato G, Polettini E, et al. (2010) Celiac disease: evaluation with dynamic contrast-enhanced MR imaging. Radiology.256(3):783-90. https://doi.org/https://doi.org/10.1148/radiol.10092160

    Article  PubMed  Google Scholar 

  21. Paolantonio P, Tomei E, Rengo M, Ferrari R, Lucchesi P, Laghi A (2007) Adult celiac disease: MRI findings. Abdom Imaging.32(4):433-40. https://doi.org/https://doi.org/10.1007/s00261-006-9089-9

    Article  PubMed  Google Scholar 

  22. Scholz FJ, Afnan J, Behr SC (2011) CT findings in adult celiac disease. Radiographics.31(4):977-92. https://doi.org/https://doi.org/10.1148/rg.314105215

    Article  PubMed  Google Scholar 

  23. Sheedy SP, Barlow JM, Fletcher JG, Smyrk TC, Scholz FJ, Codipilly DC, et al. (2017) Beyond moulage sign and TTG levels: the role of cross-sectional imaging in celiac sprue. Abdom Radiol (NY).42(2):361–88. https://doi.org/10.1007/s00261-016-1006-2

  24. Soyer P, Boudiaf M, Dray X, Fargeaudou Y, Vahedi K, Aout M, et al. (2009) CT enteroclysis features of uncomplicated celiac disease: retrospective analysis of 44 patients. Radiology.253(2):416-24. https://doi.org/https://doi.org/10.1148/radiol.2532090533

    Article  PubMed  Google Scholar 

  25. Giambelluca D, Cannizzaro F, Midiri M (2019) Jejunoileal fold pattern reversal in celiac disease. Abdom Radiol (NY).44(10):3494–5. https://doi.org/10.1007/s00261-019-02178-x

  26. Al-Bawardy B, Barlow JM, Vasconcelos RN, Kim ST, Bruining DH, Hansel SL, et al. (2017) Cross-sectional imaging in refractory celiac disease. Abdom Radiol (NY).42(2):389–95. https://doi.org/10.1007/s00261-016-1032-0

  27. Eid M, Abougabal A, Zeid A (2013) Celiac disease: Do not miss that diagnosis! Egypt J Radiol Nucl Med.44(4):727-35. https://doi.org/https://doi.org/10.1016/j.ejrnm.2013.09.010

    Article  Google Scholar 

  28. Tonutti E, Bizzaro N (2014) Diagnosis and classification of celiac disease and gluten sensitivity. Autoimmun Rev.13(4-5):472-6. https://doi.org/https://doi.org/10.1016/j.autrev.2014.01.043

    Article  CAS  PubMed  Google Scholar 

  29. van der Windt DA, Jellema P, Mulder CJ, Kneepkens CM, van der Horst HE (2010) Diagnostic testing for celiac disease among patients with abdominal symptoms: a systematic review. JAMA.303(17):1738-46. https://doi.org/https://doi.org/10.1001/jama.2010.549

    Article  PubMed  Google Scholar 

  30. Reilly NR, Fasano A, Green PH (2012) Presentation of celiac disease. Gastrointest Endosc Clin N Am.22(4):613-21. https://doi.org/https://doi.org/10.1016/j.giec.2012.07.008

    Article  PubMed  Google Scholar 

  31. Gonda TA, Khan SU, Cheng J, Lewis SK, Rubin M, Green PH (2010) Association of intussusception and celiac disease in adults. Dig Dis Sci.55(10):2899-903. https://doi.org/https://doi.org/10.1007/s10620-009-1086-8

    Article  PubMed  Google Scholar 

  32. Green PH, Cellier C (2007) Celiac disease. N Engl J Med.357(17):1731-43. https://doi.org/https://doi.org/10.1056/NEJMra071600

    Article  CAS  PubMed  Google Scholar 

  33. Freeman HJ (2010) Mesenteric lymph node cavitation syndrome. World J Gastroenterol.16(24):2991-3. https://doi.org/https://doi.org/10.3748/wjg.v16.i24.2991

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kotchetkov R, Kukreti V (2015) Cavitating Mesenteric Lymph Node Syndrome and Enteropathy-Associated T Cell Lymphoma as First Manifestation of Celiac Disease. Can J Gen Intern Med.10(3). https://doi.org/10.22374/cjgim.v10i3.47

  35. Lucey BC, Stuhlfaut JW, Soto JA (2005) Mesenteric lymph nodes seen at imaging: causes and significance. Radiographics.25(2):351-65. https://doi.org/https://doi.org/10.1148/rg.252045108

    Article  PubMed  Google Scholar 

  36. van Gils T, Nijeboer P, van Waesberghe JHT, Coupe VM, Janssen K, Zegers JA, et al. (2017) Splenic volume differentiates complicated and non-complicated celiac disease. United European Gastroenterol J.5(3):374-9. https://doi.org/https://doi.org/10.1177/2050640616663571

    Article  PubMed  Google Scholar 

  37. 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):786-90. https://doi.org/https://doi.org/10.2214/AJR.07.2109

    Article  PubMed  Google Scholar 

  38. Moser PP, Smith JK (2004) CT findings of increased splanchnic circulation in a case of celiac sprue. Abdom Imaging.29(1):15-7. https://doi.org/https://doi.org/10.1007/s00261-003-0084-0

    Article  CAS  PubMed  Google Scholar 

  39. Martel J, Sussman DA, Goldberg RI, Valantas M, Barkin JS (2009) Benign small bowel thickening and lymphadenopathy: a manifestation of celiac disease. Dig Dis Sci.54(4):902-5. https://doi.org/https://doi.org/10.1007/s10620-008-0426-4

    Article  PubMed  Google Scholar 

  40. 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):575-7. https://doi.org/https://doi.org/10.2214/ajr.166.3.8623630

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Radiology, Medical Faculty, Van Yüzüncü Yıl University, Van, Turkey

    Cemil Göya, İlyas Dündar, Mesut Özgökçe, Ensar Türko, Sercan Özkaçmaz & Fatma Durmaz

  2. Department of Internal Medicine, Medical Faculty, Van Yüzüncü Yıl University, Van, Turkey

    Mesut Aydın, Yusuf Geylani & Mehmet Arslan

  3. Department of Pathology, Medical Faculty, Dicle University, Diyarbakır, Turkey

    Ulaş Alabalık

  4. Department of Radiology, Medical Faculty, Dicle University, Diyarbakır, Turkey

    Salih Hattapoğlu

  5. Department of Radiology, Dursun Odabasi Medical Center, Van Yuzuncu Yil University, Campus, Tusba, 65080, Van, Turkey

    İlyas Dündar

Authors
  1. Cemil Göya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. İlyas Dündar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mesut Özgökçe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ensar Türko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sercan Özkaçmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fatma Durmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mesut Aydın
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ulaş Alabalık
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yusuf Geylani
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mehmet Arslan
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Salih Hattapoğlu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CG: Conceptualization, Writing—Original Draft, Formal analysis, Project administration, Supervision. İD: Software, Data Curation, Visualization, Writing—Review and Editing. MÖ: Validation, Writing—Review and Editing, Formal analysis. ET: Resources, Data Curation, Visualization, Investigation. SÖ: Data Curation, Software, Visualization. FD: Data Curation, Software, Investigation. MA: Investigation, Data Curation. UA: Resources, Methodology, Data Curation. YG: Investigation, Data Curation. MA: Data Curation, Software. SH: Resources, Data Curation, Validation.

Corresponding author

Correspondence to İlyas Dündar.

Ethics declarations

Conflict of ınterest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Göya, C., Dündar, İ., Özgökçe, M. et al. Does contrast-enhanced computed tomography raise awareness in the diagnosis of the invisible side of celiac disease in adults?. Abdom Radiol 47, 1750–1761 (2022). https://doi.org/10.1007/s00261-022-03480-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00261-022-03480-x

Keywords

Search

Navigation