CT Findings in Malabsorptive Bowel Disease

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1 CT Findings in Malabsorptive Bowel Disease Poster No.: C-2142 Congress: ECR 2015 Type: Educational Exhibit Authors: H. Rodriguez Requena; Madrid/ES Keywords: Motility, Inflammation, Education and training, Observer performance, Education, Contrast agent-oral, CT, Small bowel, Gastrointestinal tract, Abdomen DOI: /ecr2015/C-2142 Any information contained in this pdf file is automatically generated from digital material submitted to EPOS by third parties in the form of scientific presentations. References to any names, marks, products, or services of third parties or hypertext links to thirdparty sites or information are provided solely as a convenience to you and do not in any way constitute or imply ECR's endorsement, sponsorship or recommendation of the third party, information, product or service. ECR is not responsible for the content of these pages and does not make any representations regarding the content or accuracy of material in this file. As per copyright regulations, any unauthorised use of the material or parts thereof as well as commercial reproduction or multiple distribution by any traditional or electronically based reproduction/publication method ist strictly prohibited. You agree to defend, indemnify, and hold ECR harmless from and against any and all claims, damages, costs, and expenses, including attorneys' fees, arising from or related to your use of these pages. Please note: Links to movies, ppt slideshows and any other multimedia files are not available in the pdf version of presentations. Page 1 of 66

2 Learning objectives Celiac Disease is a chronic autoimmune condition in which the immune system responds abnormally to gluten in genetically predisposed patients. It primarily affects the small bowel mucosa, causing inflammation at first, and destruction and crypt hyperplasia on later stages, leading to malabsorption and fluid overload within the intestinal lumen. 1. In this exhibit we will review the characteristic malabsorptive pattern of celiac disease in CT 2. We will also describe the associated imaging findings that we can recognize that will help us establishing an early diagnosis 3. Finally we will discuss the advantages and limitations of CT versus barium studies Fig. 1: Celiac Disease Page 2 of 66

3 References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 3 of 66

4 Images for this section: Fig. 1: Celiac Disease Radiology, Hospital 12 de Octubre - Madrid/ES Page 4 of 66

5 Background 1. EPIDEMIOLOGY Celiac Disease (CD) is a common condition in our environment, although recent epidemiological studies have demonstrated that CD prevalence is still underestimated (1). There is a large proportion of celiacs that remain undiagnosed. This is due, in part, to many clinicians being unfamiliar with the condition and also due to the fact that it can be asymptomatic. Recent increases in the number of reported cases may be explained by changes in diagnostic practice and different design of population studies (2) have also shown the development of antibodies in elderly people increasing prevalence in Western Societies., but recent studies (3), leading it all to an Page 5 of 66

6 Fig. 2: Changes in the design of prevalence studies of CD (3) References: Radiology, Hospital 12 de Octubre - Madrid/ES Population studies have shown that the overall CD prevalence is 1.0%, varying between (4) 0.33 and 1.06% in children and % in adults. There is an increasing prevalence in adults, ranging from 2.4% in Northern Europe, to 0.3% in Germany and 0.7% in Italy (5), among subjects aged years, and a rising portion of CD patients diagnosed after the age of 65 years, as mentioned before. Also, there is marked geographical variation in CD incidence and prevalence around the world, with a higher prevalence in Western Caucasian Populations, explained by the different prevalence of HLA susceptibility alleles and diversity in nutritional practices (2). 2. SIGNS AND SYMPTOMS Celiac disease can cause a wide spectrum of symptoms ranging from a subclinical form, which may be incidentally detected, to the classic malabsorptive form (Table 1). Symptoms can be nonspecific, leading a delay in its accurate diagnosis since the beginning of its first manifestations, and so causing a higher morbidity and mortality. Page 6 of 66

7 Table 1: Clinical findings in CD References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 7 of 66

8 Fig. 3: 55 year old patient with long standing CD. CT shows the so called "reverse fold pattern", with thickening of the walls and folds of ileum References: Radiology, Hospital 12 de Octubre - Madrid/ES CD is associated to an increased risk of both adenocarcinoma and lymphoma of the small bowel (figs. 4, 5 and 6), being the most common cause of death in celiac patients, who have a double mortality rate than general population (6). There are a subset of patients with refractory disease (defined as a symptomatic severe enteritis that does not respond to at least 6 months of a strict gluten-free diet) who are Page 8 of 66

9 prone to suffer complications from the disease (Table 2. Fig. 7), as well as those patients with untreated disease. Table 2: Complications in CD References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 9 of 66

10 Fig. 4: Same patient as figure 3, showing enlarged mesenteric lymph nodes. Intestinal biopsy was performed, showing an increased celularity in the lamina propria. Suspicion of associated lymphoproliferative disorder was raised. References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 10 of 66

11 Fig. 5: 43 year old male with CD. CT reveals segmental wall thickening of the small bowel with aneurysmatic dilatation, a finding suggestive of intestinal lymphoma, later confirmed by biopsy References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 11 of 66

12 Fig. 6: Same patient as figure 5, showing lymphomatous involvement of another bowel segment References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 12 of 66

13 Fig. 7: 61 year old patient with CD, routine follow up CT revealed pneumatosis in small bowel loops in the left flank. As he was asymptomatic, conservative management was established References: Radiology, Hospital 12 de Octubre - Madrid/ES 3. SPECIAL FOCUS IN ELDERLY PATIENTS Page 13 of 66

14 Recent studies describe an increasing prevalence of celiac disease with age: some have documented that 15 percent of newly diagnosed patients are older than 65 years, with (7) symptoms lasting for 10 years prior to correct diagnosis, and other studies showing a prevalence of biopsy proven celiac disease of 2 percent for individuals aged between 52 and 74 (3). In our common practice, CD is not a well recognized entity in elderly patients, in part due to a lack of suspicion by both clinicians and radiologists, but also because of the usual paucity of symptoms in this particular population. Presentation of CD may be subtle, with few abdominal complaints or lack of them, and showing only general and vague complaints. Anemia due to malabsorption of different nutrients may be also the one and only abnormality in laboratory tests. Fig. 8 References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 14 of 66

15 Therefore, radiologists should be really aware of this condition when receiving a request for an abdominal CT in this particular setting, to appropriate programme the study and, mainly, include CD in their differential (fig. 9). Fig. 9: 85 year old lady admitted at our institution for iron deficiency anemia workup, with only salient finding in abdominal CT being a small spleen. Suspicion of CD was raised by the radiologist, not confirmed so far. Page 15 of 66

16 References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 16 of 66

17 Images for this section: Fig. 2: Changes in the design of prevalence studies of CD (3) Radiology, Hospital 12 de Octubre - Madrid/ES Page 17 of 66

18 Table 1: Clinical findings in CD Radiology, Hospital 12 de Octubre - Madrid/ES Page 18 of 66

19 Fig. 3: 55 year old patient with long standing CD. CT shows the so called "reverse fold pattern", with thickening of the walls and folds of ileum Radiology, Hospital 12 de Octubre - Madrid/ES Page 19 of 66

20 Table 2: Complications in CD Radiology, Hospital 12 de Octubre - Madrid/ES Page 20 of 66

21 Fig. 4: Same patient as figure 3, showing enlarged mesenteric lymph nodes. Intestinal biopsy was performed, showing an increased celularity in the lamina propria. Suspicion of associated lymphoproliferative disorder was raised. Radiology, Hospital 12 de Octubre - Madrid/ES Page 21 of 66

22 Fig. 5: 43 year old male with CD. CT reveals segmental wall thickening of the small bowel with aneurysmatic dilatation, a finding suggestive of intestinal lymphoma, later confirmed by biopsy Radiology, Hospital 12 de Octubre - Madrid/ES Page 22 of 66

23 Fig. 6: Same patient as figure 5, showing lymphomatous involvement of another bowel segment Radiology, Hospital 12 de Octubre - Madrid/ES Page 23 of 66

24 Fig. 7: 61 year old patient with CD, routine follow up CT revealed pneumatosis in small bowel loops in the left flank. As he was asymptomatic, conservative management was established Radiology, Hospital 12 de Octubre - Madrid/ES Page 24 of 66

25 Fig. 8 Radiology, Hospital 12 de Octubre - Madrid/ES Page 25 of 66

26 Fig. 9: 85 year old lady admitted at our institution for iron deficiency anemia workup, with only salient finding in abdominal CT being a small spleen. Suspicion of CD was raised by the radiologist, not confirmed so far. Radiology, Hospital 12 de Octubre - Madrid/ES Page 26 of 66

27 Findings and procedure details The use of barium studies has fallen into disuse in our current practice, with fewer explorations requested by clinicians over the past two decades, as a result of greater utilization of modern modalities, with MR and CT optimized for small bowel imaging (8) playing an important and increasing role. Being the amount of studies less and less, training of radiology residents has been significantly affected even in teaching Hospitals and that, together with the retirement of expert radiologist without a sufficient replacement, is leading to a meaningful reduction of specialists in its performance and interpretation. Now is our time to adapt and evolve, using our current and more available techniques to diagnose a tricky condition such as CD, being our responsibility as radiologists not to overlook this entity, often not suspected or properly recognized due to the variety of clinical settings. This haziness may lead to a significant delay in diagnosis, proved to be as high as 10 years from onset of symptoms in one study of serious complications. (9), and hence raising the rate In this scenario, CT has become an essential diagnostic tool, both in patients suspected to have a celiac disease as well as in those with non specific abdominal complaints. CT (10) provides detailed information on the bowel wall and extraenteric structures, allowing the diagnosis of CD being suggested by the radiologist, prompting further evaluations and therefore coming to a definitive diagnosis, with subsequent initiation of the appropriate treatment, which is necessary to prevent the significant morbidity and increased mortality associated with untreated situations. Page 27 of 66

28 Fig. 10: 60 year old male with known history of CD. Note the wall thickening in duodenum, which is an unusual finding in this disease. References: Radiology, Hospital 12 de Octubre - Madrid/ES However, definite diagnosis must be made on the basis of histological confirmation and favorable response to gluten-free diet. 1. PROCEDURE DETAILS Page 28 of 66

29 Optimal distention of the small bowel loops is essential for an appropriate assessment of bowel wall, as collapsed loops can hide lesions or mimic disease. To achieve an adequate repletion, some institutions advocate for the use of CT enterography, using neutral or low - density oral contrast media, obtaining excellent filling of bowel lumen and great (10) depiction of mucosal detail and occasional narrowings. Others have experience with CT enteroclysis, offering a better distention and higher accuracy detecting complications of CD, having been proved to exclude small-bowel stricture before wireless capsule endoscopy, and consequently limiting the risk of capsule retention (11, 12). We prefer to use an opaque water soluble agent, to evaluate not only the bowel wall but also features associated with contrast itself, and so obtaining further information, as later will be explained. CT scans should be performed with the patient in the supine position, fasting for at least 4 to 6 hours, with no other special preparation on previous days. Intravenous and opaque oral contrast agent is administered in all patients (Gastrografin, Diatrizoate Meglumine and Diatrizoate Sodium Solution USP, Bayern Hispania), avoiding the use of barium-based contrast agents, as these are specifically designed to retain intraluminal fluid, being counter - productive for our goal. Helical acquisition is performed from the diaphragm to the pubis, beginning 70 seconds after the administration of intravenous contrast material (venous phase). We use either both a Philips Brilliance CT 64-channel (Philips Healthcare, Koninklijke Philips N.V.) and a Siemens Somatom Sensation CT 16-channel (Siemens Healthcare, Siemens AG), with standard acquisition parameters for abdominal studies (slice collimation 16 x 1.5 mm, slice width 3 mm, rotation time 0.5 seconds). Images are evaluated in workstations equipped with Philips IntelliSpace Portal, a multimodality viewing application with the usual post-processing tools. 2. IMAGING FINDINGS Throughout this review, we will portray the characteristic malabsorptive pattern of celiac disease as well as the associated imaging findings that we can recognize in CT, that allow us establishing an early diagnosis. These findings have been well documented in the literature (10, 11, 12, 13, 14). A) SMALL BOWEL ABNORMALITIES: Page 29 of 66

30 The underlying pathophysiology in CD is an autoimmune response to gluten, leading to a progressive lymphocytic infiltration of the small bowel epithelium and subsequent villous atrophy, followed by crypt hyperplasia, in genetic predisposed patients. Involvement of small bowel is variable, beginning in the duodenum and proximal jejunum, and advancing distally later on. These changes are graded according to the Marsh score (fig. 11) and, as previously stated, histological confirmation is needed to determine a diagnosis of CD. Fig. 11: Marsh Grading System References: Radiology, Hospital 12 de Octubre - Madrid/ES Chronic inflammation of small bowel epithelium leads to a fluid overload in the lumen by two paths: first, a reduction in the amount of liquid that villi are able to absorb due to its atrophy, and secondary, an excess in fluid production caused by the hypertrophy of the crypts. Page 30 of 66

31 Most of the features of the classic malabsorption pattern recognized in CT are directly or indirectly related with this excess of fluid (summarized in Table 3). Table 3: Small bowel findings References: Radiology, Hospital 12 de Octubre - Madrid/ES 1- Dilatation of small bowel loops (fig. 12) is caused by the aforementioned excess (13) of intraintestinal fluid, being a common finding, seen up to 75% of CD patients. This dilatation is uniform and does not lead to secondary distention of small bowel, without additional data of obstruction, needless to mention. As disease begins in duodenum and jejunum and advances distally, depending on the time in its natural history when the scan is performed, we can find a segmental or diffuse involvement. Page 31 of 66

32 Fig. 12: Dilatation of proximal jejunum loops References: Radiology, Hospital 12 de Octubre - Madrid/ES 2- Reversed jejuno-ileal fold pattern (figs. 13 and 14), showing a partial or complete loss of usual folding pattern of the proximal small bowel due to a severe villous atrophy, combined with an unusually increased one in the ileum, probably as a compensatory response. This is the most specific abnormality found in CD reformatted images to achieve a better depiction. (13), and we can use coronal Page 32 of 66

33 Fig. 13: 53 year old female with known CD. Note the "reversed fold pattern", with "jejunization" of pelvic ileum loops References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 33 of 66

34 Fig. 14: Same patient as fig.13. Coronal reformatted image References: Radiology, Hospital 12 de Octubre - Madrid/ES 3- Conglomeration of small bowel loops (fig. 15) can be seen, specially in the pelvis, with loops conforming one against each other. In advanced phases of the disease, dilated small bowel loops end up losing their muscular tone after a long struggle against unusual intraluminal liquid overload. This flaccid and fluid - filled loops tight together mainly in the pelvis, where there are less restrictions, occupying and filing all empty spaces, with no spare fat visualized between adjacent loops. Page 34 of 66

35 Fig. 15: 55 year old patient with recent diagnosis of CD. CT shows conglomeration of ileal loops in the pelvis. Note also oral contrast dilution References: Radiology, Hospital 12 de Octubre - Madrid/ES 4- Telescoping (figs. 16 and 17) and occasionally transient intus-susception (fig. 18), also as a result of the progressive loss of normal muscular tone previously explained, and likewise due to an uncoordinated peristalsis. These flaccid loops are seen with a "target" appearance on axial images, representing crowding of remnant folds in the lumen, without accompanying mesenteric fat and vessels. Intussusception, reflecting a further feature of the same process, can also be detected, being usually asymptomatic Page 35 of 66

36 and self - limiting and so requiring no more intervention. It is essential, however, to exclude a secondary cause of the intussusception in these patients, as it can be produced by a neoplasm. Fig. 16: Proximal jejunal loop showing a "target" appearance of the wall (open arrow), in a 48 year old patient with celiac disease References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 36 of 66

37 Fig. 17: Another example of telescoping, with "target" appearance of small bowel loop in the right flank (open arrow), in a 52 year old celiac References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 37 of 66

38 Fig. 18: Transient intussusception in left iliac fossa of a 52 year old asymptomatic CD patient References: Radiology, Hospital 12 de Octubre - Madrid/ES 5- The presence of intramural fat (figs. 19 and 20) in the submucosa of the proximal bowel (duodenum and jejunum) has been reported to be a highly suggestive finding of CD (15). Destruction of the protective villous lining of the proximal bowel predisposes to insult from gastric, biliary, and pancreatic secretions, with subsequent intramural fat deposition as a response to prior inflammation. Page 38 of 66

39 Fig. 19: 48 year old CD patient with intramural fat in duodenum (open arrow) References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 39 of 66

40 Fig. 20: Same patient as fig. 19, showing involvement of distal duodenum References: Radiology, Hospital 12 de Octubre - Madrid/ES 6- Oral contrast dilution (figs. 15 and 21) can be detected in the lumen of the small bowel, in the setting of fluid overload, as well as flocculation (fig. 22) of oral contrast material, seen as small clusters of oral contrast on dependent portion of dilated bowel loops. Page 40 of 66

41 Fig. 21: Dilution of oral contrast material in dilated loops of proximal jejunum References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 41 of 66

42 Fig. 22: 53 year old female with CD (same as fig. 13). CT shows flocculation of oral contrast material, seen as irregular dots of oral contrast precipitating in the dilated bowel loops (open arrow) References: Radiology, Hospital 12 de Octubre - Madrid/ES B) ASSOCIATED FINDINGS: Cross sectional imaging (either CT or MR) provide a significant advantage over classical barium studies: ancillary features can be detected outside the bowel, raising the suspicion of CD and helping establishing a reliable radiological diagnosis. Page 42 of 66

43 1- Small spleen: although a rather nonspecific finding, seen in many other conditions, hyposplenism (figs. 9 and 23 ) can be found up to 30-50% adult patients with CD, and the (11) extent of splenic atrophy is associated with the severity of the disease. This feature may be a part of a triad, together with a severe villous atrophy and hypoattenuating lymphadenopathies, defining the so called cavitary mesenteric lymph node syndrome, an unusual complication of CD, that may be associated with lymphoma. Fig. 23: 56 year old patient with CD and associated hyposplenism Page 43 of 66

44 References: Radiology, Hospital 12 de Octubre - Madrid/ES 2- Mesenteric lymphadenomegaly, reflecting follicular hyperplasia secondary to an abnormal proliferation of reactive lymphocytes in the lymph nodes, caused by the autoimmune cascade. Mesenteric lymph node prominence is such a common finding in abdominal imaging, associated with a wide range of benign and malignant disorders, and may be subtle in CD. This ties with the lack of consensus regarding its pathologic size, apart from the 10 mm short axis diameter established by the RECIST criteria in (16) oncologic patients, that is why they may be overlooked if not carefully evaluated. Lymphadenopathies in CD appear generally around the first bowel segments (duodenum and jejunum. Fig. 24), where the disease is more active, as opposite to other entities that tend to affect the distal bowel (mesenteric adenitis, Crohn disease). Page 44 of 66

45 Fig. 24: Same patient as fig. 23, showing also prominent mesenteric lymphadenopathies References: Radiology, Hospital 12 de Octubre - Madrid/ES 3- Vascular engorgement, is also a secondary finding that can be present in multiple bowel diseases, usually indicating hypervascularity in the bowel wall. In CD is specially obvious during the active phase of the disease (fig. 25). Page 45 of 66

46 Fig. 25: Same patient as figs. 23 and 24, showing also an engorged superior mesenteric vein (open arrow) References: Radiology, Hospital 12 de Octubre - Madrid/ES Page 46 of 66

47 Images for this section: Fig. 10: 60 year old male with known history of CD. Note the wall thickening in duodenum, which is an unusual finding in this disease. Radiology, Hospital 12 de Octubre - Madrid/ES Page 47 of 66

48 Table 3: Small bowel findings Radiology, Hospital 12 de Octubre - Madrid/ES Page 48 of 66

49 Fig. 11: Marsh Grading System Radiology, Hospital 12 de Octubre - Madrid/ES Page 49 of 66

50 Fig. 12: Dilatation of proximal jejunum loops Radiology, Hospital 12 de Octubre - Madrid/ES Page 50 of 66

51 Fig. 13: 53 year old female with known CD. Note the "reversed fold pattern", with "jejunization" of pelvic ileum loops Radiology, Hospital 12 de Octubre - Madrid/ES Page 51 of 66

52 Fig. 14: Same patient as fig.13. Coronal reformatted image Radiology, Hospital 12 de Octubre - Madrid/ES Page 52 of 66

53 Fig. 15: 55 year old patient with recent diagnosis of CD. CT shows conglomeration of ileal loops in the pelvis. Note also oral contrast dilution Radiology, Hospital 12 de Octubre - Madrid/ES Page 53 of 66

54 Fig. 16: Proximal jejunal loop showing a "target" appearance of the wall (open arrow), in a 48 year old patient with celiac disease Radiology, Hospital 12 de Octubre - Madrid/ES Page 54 of 66

55 Fig. 17: Another example of telescoping, with "target" appearance of small bowel loop in the right flank (open arrow), in a 52 year old celiac Radiology, Hospital 12 de Octubre - Madrid/ES Page 55 of 66

56 Fig. 18: Transient intussusception in left iliac fossa of a 52 year old asymptomatic CD patient Radiology, Hospital 12 de Octubre - Madrid/ES Page 56 of 66

57 Fig. 19: 48 year old CD patient with intramural fat in duodenum (open arrow) Radiology, Hospital 12 de Octubre - Madrid/ES Page 57 of 66

58 Fig. 20: Same patient as fig. 19, showing involvement of distal duodenum Radiology, Hospital 12 de Octubre - Madrid/ES Page 58 of 66

59 Fig. 21: Dilution of oral contrast material in dilated loops of proximal jejunum Radiology, Hospital 12 de Octubre - Madrid/ES Page 59 of 66

60 Fig. 22: 53 year old female with CD (same as fig. 13). CT shows flocculation of oral contrast material, seen as irregular dots of oral contrast precipitating in the dilated bowel loops (open arrow) Radiology, Hospital 12 de Octubre - Madrid/ES Page 60 of 66

61 Fig. 23: 56 year old patient with CD and associated hyposplenism Radiology, Hospital 12 de Octubre - Madrid/ES Page 61 of 66

62 Fig. 24: Same patient as fig. 23, showing also prominent mesenteric lymphadenopathies Radiology, Hospital 12 de Octubre - Madrid/ES Page 62 of 66

63 Fig. 25: Same patient as figs. 23 and 24, showing also an engorged superior mesenteric vein (open arrow) Radiology, Hospital 12 de Octubre - Madrid/ES Page 63 of 66

64 Conclusion There is an increasing prevalence of celiac disease in our environment, with recent studies even describing a "non-celiac gluten sensitivity", a disorder showing some morphological, immunological, or functional abnormalities that improve after gluten removal, but not completely fulfilling the histologic criteria of CD (17). A delay in its accurate diagnosis leads to a higher morbidity, developing serious complications after long standing disease, that may be potentially fatal if untreated. In this context, knowledge of the classic CT malabsorption pattern in the small bowel and of the ancillary findings is mandatory to establish an early diagnosis of CD, taking into account the current disuse of barium studies in our daily practice. Awareness of this condition is crucial for radiologists to establish an adequate CT protocol and actively search for the described features of this disease, specially in a subset of elderly patients with faint abdominal complaints or anemia, in which the suspicion is not clearly specified by their requesting clinician. Page 64 of 66

65 Personal information Thank you very much for your attention! For contact, please address to: Hugo Rodríguez Requena, Page 65 of 66

66 References Altobelli E, Paduano R, Petrocelli R, Di Orio F. Burden of Celiac Disease in Europe: a review of its childhood and adulthood prevalence and incidence as of September Ann Ig Nov-Dec; 26(6): Polanco I. Enfermedad Celiaca. Presente y Futuro Ed Ergon Vilppula A, Kaukinen K, Luostarinen L, et al. Increasing prevalence and high incidence of celiac disease in elderly people: a population-based study. BMC Gastroenterol. 2009; 9: 49 Van Heel DA, West J. Recent advances in coeliac disease. Gut Jul. 55 (7): Mustalahti K et al. The prevalence of celiac disease in Europe: results of a centralized, international mass screening project. Ann Med Dec; 42(8): Logan RF, Rifkind EA, Turner ID, Ferguson A. Mortality rate in celiac disease. Gastroenterology. 1989; 97: Patel D, Kalkat P, Baisch D, Zipser R. Celiac disease in the elderly. Gerontology 2005; 51:213 Levine MS. Colon and Rectum Barium Studies. Abdominal Imaging. 2013, pp Norström F, Lindholm L, Sandström O, Nordyke K, Ivarsson A. Delay to celiac disease diagnosis and its implications for health-related quality of life. BMC Gastroenterol Nov 7;11:118. Masselli G, Gualdi G. CT and MR enterography in evaluating small bowel diseases: when to use which modality?. Abdom Imaging. 2013; 38: Soyer P. et al. Celiac Disease in Adults: Evaluation with MDCT Enteroclysis. AJR. 2008; 191: Boudiaf M, Jaff A, Soyer P, Bouhnik Y, Hamzi L, Rymer R. Smallbowel diseases: prospective evaluation of multi-detector row helical CT enteroclysis in 107 consecutive patients. Radiology 2004; 233: Tomei E. et al. Abdominal CT findings may suggest coeliac disease. Dig Liver Dis Jun;37(6): Scholz FJ, Afnan J, Behr SC. CT Findings in Adult Celiac Disease. RadioGraphics 2011; 31: Scholz FJ, Behr SC, Scheirey CD. Intramural fat in the duodenum and proximal small intestine in patients with celiac disease. AJR 2007; 189: Chalian H et al. Radiologic Assessment of Response to Therapy: Comparison of RECIST Versions 1.1 and RadioGraphics 2011; 31: Verdú EF, Armstrong D, Murray JA. Between Celiac Disease and Irritable Bowel Syndrome: The "No Man's Land" of Gluten Sensitivity. Am J Gastroenterol. Jun 2009; 104(6): Page 66 of 66

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