CT Findings in Adult Celiac Disease 1

Note:  This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, cont...
0 downloads 1 Views 4MB Size
Note:  This copy is for your personal non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights.



CT Findings in Adult Celiac Disease1 CME FEATURE See www.rsna .org/education /rg_cme.html

LEARNING OBJECTIVES FOR TEST 4 After completing this journal-based CME activity, participants will be able to: ■■Discuss

the increasing prevalence of celiac disease in the U.S. population, its acute presentation, and its associated morbidity and mortality. ■■List

the intra- and extraintestinal manifestations of celiac disease and describe its underlying pathophysiology. ■■Describe

the role of the radiologist in recognizing the malabsorptive process, particularly in celiac disease, and suggesting appropriate follow-up.

Francis J. Scholz, MD • Jalil Afnan, MD • Spencer C. Behr, MD Celiac disease is now recognized as a common disease, occurring in about one in every 200 Americans. However, less than 10% of cases are currently diagnosed, with a diagnostic delay of more than 10 years from onset of symptoms. In the past, barium examination of the small bowel demonstrated a pattern of abnormal findings caused by the pathophysiologic changes induced by malabsorption, thus leading to diagnosis of celiac disease and other diseases of malabsorption. Although not specific, that pattern prompted further patient evaluation. The number of barium examinations performed and the skill necessary to interpret their results are both in decline. Abdominal pain in celiac disease is a common early complaint that often leads to computed tomography (CT). Improved CT resolution now permits better depiction of the small bowel, colon, and mesenteric lymph nodes, all of which are affected by celiac disease. Detection of celiac disease with CT will allow treatment to be initiated to prevent the significant morbidity and increased mortality associated with a delay in diagnosis. The abnormal CT findings seen over the past decade during review of more than 200 cases of celiac disease demonstrate that CT depicts more features of celiac disease than did barium examination. Pattern recognition for the diagnosis of small bowel diseases that create structural changes in the bowel wall is well accepted. Because it demonstrates features of celiac disease not detected with barium examination, CT may be more sensitive than barium examination for diagnosis of this disease. ©

RSNA, 2011 • radiographics.rsna.org

Abbreviation: MABP = malabsorption pattern RadioGraphics 2011; 31:977–992 • Published online 10.1148/rg.314105215 • Content Codes: From the Department of Radiology, Lahey Clinic, 41 Mall Rd, Burlington, MA 01803. Recipient of a Certificate of Merit award for an education exhibit at the 2009 RSNA Annual Meeting. Received October 7, 2010; revision requested November 19 and received January 11, 2011; accepted January 31. For this journal-based CME activity, the authors (J.A., S.C.B.), editor, and reviewers have no relevant relationships to disclose. F.J.S. is the owner of FSpoon Co. Address correspondence to F.J.S. (e-mail: [email protected]). 1


RSNA, 2011

978  July-August 2011


Celiac disease is now recognized as a common disease, occurring in about 1 in every 200 Americans (1). However, less than 10% of cases are currently diagnosed (2), with a diagnostic delay of more than 10 years from onset of symptoms. Celiac disease is a chronic autoimmune disorder induced in genetically susceptible individuals after ingestion of gluten proteins, which are found in wheat, rye, barley, and certain other grains. The small bowel mucosa is primarily affected, resulting in progressive degrees of villus inflammation and destruction with resulting induction of crypt hyperplasia (3). The destruction begins in the duodenum and over time progresses distally to the ileum. Loss of villi, which absorb fluid, and hypertrophy of crypts, which produce fluid, result in chronic fluid excess in the small bowel lumen (4). Chronic excess fluid and its effects on bowel wall structure and tone create the small bowel malabsorption pattern (MABP), which was described long ago in barium studies of patients with celiac disease (5,6). Features of the celiac disease MABP include duodenitis (7) (Fig 1a), dilution, dilatation, slow transit, flocculation (Fig 1b), moulage (Fig 1c), reversal of the jejunalileal fold pattern (8) (Fig 1d), and transient small bowel intussusception. Unfortunately, this barium examination pattern is not specific (9,10), and barium studies of the small bowel are no longer commonly performed. If celiac disease is suspected, confirmation or evaluation with endoscopy, antibody testing, or even computed tomographic (CT) enteroclysis may be performed to stage the severity of the disease (11). Antibody testing has been shown to be both sensitive and highly specific for anti– tissue transglutaminase and anti-endomysial antibodies (12). However, it is necessary to establish initial suspicion, and this is problematic in clinical practice. Pain, a frequent indication for CT, is also a common clinical feature of celiac disease (13). Identifying the CT features of the MABP will allow the diagnosis of celiac disease to be suggested in patients undergoing CT for pain or any other indication. Detection of celiac disease with CT will allow treatment to be initiated to prevent the significant morbidity (14,15) and increased mortality (16) associated with a delay in diagnosis. Individual CT features of celiac disease (17–20) or findings at CT enterography of patients with known celiac disease (21) have been described. However, few authors have attempted to describe or illustrate a comprehensive CT pat-


tern that can be used to diagnose unknown celiac disease during an initial examination (22–24). Pattern recognition for diagnosis of small bowel diseases that create structural changes in the small bowel wall is well accepted (22,25). In this article, we present and illustrate a pattern of CT findings in celiac disease that allows the diagnosis to be made. The celiac disease pattern has several components: the small bowel MABP, mesenteric lymph node prominence in the small bowel, and the colonic MABP. Additional CT findings in celiac disease together with these components increase the likelihood of making the diagnosis. The full pattern of CT findings that allows diagnosis of celiac disease is shown.

Selection of CT Studies

A study was performed to understand the spectrum of CT findings in celiac disease. After approval by the institutional review board, results of all antibody tests for celiac disease performed at our institution from the inception of testing in 1996 to 2009 were obtained. All tests with positive results were used to find abdominal CT scans in the picture archiving and communication system; the total was approximately 200 studies. The findings on all CT scans were reviewed and serve as the basis for this article. Chart records were reviewed to discover coexisting conditions. Scans were not used if a coexisting condition that may affect the bowel was noted. Lupus erythematosus, bowel surgery, abdominal tumors, cirrhosis, radiation therapy, chemotherapy, and inflammatory bowel disease are examples of entities that prompted exclusion. Scans obtained with oral opaque contrast material, with or without intravenous contrast material, were used. Results of examinations with Volumen (barium sulfate; E-Z-Em, Westbury, NY) were excluded. This agent was designed specifically to maintain intraluminal fluid and bowel distention. Because disturbance in small bowel fluid physiology is the basis of an MABP, use of this agent precludes physiologic evaluation of the small bowel. It was not possible to correlate the CT findings with disease activity, positive antibody titer level, severity of biopsy results, or whether the CT study was performed before or after the diagnosis of celiac disease was made.

Clinical Presentation

Once thought to be a relatively rare diarrheaassociated debilitating disease affecting 1 in 10,000–30,000 individuals, primarily children, celiac disease is now estimated to occur in 1 in 200 Americans of any age (26). Previously prevailing ideas about the clinical presentation

RG  •  Volume 31  Number 4

Scholz et al  979

Figure 1.  Findings of malabsorption at barium examination. (a) Image shows duodenitis with nodularity in a fold-free duodenum (arrow). (b) Image shows flocculation (within oval at upper right), dilution (single arrow), and dilatation (double arrow). (c) Image shows moulage (within oval), which is a featureless bald appearance of the jejunum caused by atrophy of folds and wall edema. (d) Image shows reversal of the fold pattern (within oval), with more prominent folds in the ileum than in the jejunum.

of celiac disease are now challenged by studies demonstrating that diarrhea is seen in less than 20% of patients (27), while constipation is present in 15%. Furthermore, weight loss is rare. Most patients are of normal weight, only 5% are underweight, 39% are overweight, and 13% are obese at presentation (28). Abdominal pain, iron deficiency anemia, and guaiac-positive stools (29) are considered common presenting symptoms. It is now recognized that if

diagnosis is delayed for more than a decade from the time symptoms develop, there is increased morbidity (including iron deficiency anemia, lactose intolerance, osteoporosis, increased fracture risk, miscarriage, low birth weight, lymphoma, seizures, and depression) and increased mortality. Studies show a fourfold increase in deaths during a 45-year follow-up of undiagnosed cases (1).

980  July-August 2011


Figure 2.  Marsh grading system (3). In stage 0 (the preinfiltrative stage), there are typical small bowel villi with normal-appearing mucosa. In stage 1 (the infiltrative stage), there is a mild increase in intraepithelial lymphocytes. In stage 2 (the infiltrative hyperplastic stage), there is marked lymphocytic infiltration, mucosal edema, and proliferation of the crypts of Lieberkühn. In stage 3 (the flat destructive stage), there is partial or complete villous atrophy. In stage 4 (the atrophic hypoplastic stage), there is hypoplasia of the small bowel architecture. Progressive lymphadenopathy is seen throughout the various stages.

Table 1 MABP in the Small Bowel and Colon Small bowel MABP   Excess fluid in the small bowel   Fluid-filled loops   Dilution   Flocculation   Laminar flow   Dilated small bowel   Large volume   Telescoping   Intussusception   Conformation Colonic MABP   Large volume: a large colon from chronic gas production   Fluid plume in the right colon: small bowel fluid pours into a flaccid right colon   Encrusted right colon wall: adherent stool produces an irregular wall   Flatus, often flagrant: unabsorbed nutrients produce colon gas   Fat attenuation fluid or stool: imaging with lung windows may show that some of   the gas is actually fatty fluid   Geodes: crusted round stool balls in the left colon that contain fat and gas; the stool   surface may calcify


The autoimmune destruction of small bowel villi is a histologic diagnosis; the degree of inflammatory infiltrate and villous atrophy is quantified with the Marsh grading system (3) (Fig 2). Stage 0 is the quiescent phase, during which biopsy results and the clinical state are normal. During the attack phases of stages 1 and 2, progressive lymphocytic infiltration is noted. This will produce nodular and thickened duodenal and jejunal folds (30).

During the destructive stage 3, chronic excess intraluminal fluid stretches the small bowel, delaying transit and resulting in small bowel malabsorption. In the atrophic stage 4, there is complete villous atrophy and crypt hyperplasia with progression to wall thinning. As the jejunal mucosa and the absorptive capacity are destroyed, the ileum is exposed to gluten. The ileal folds become inflamed and thickened by progression of the autoimmune process, producing the jejunoileal fold reversal. The advanced small bowel disease overwhelms the fluid-absorbing capacity of the colon, resulting in diarrhea.

RG  •  Volume 31  Number 4

Figure 3.  Fluid-filled small bowel loops in a patient with celiac disease. CT image obtained with opaque oral contrast material shows fluid-filled bowel loops (arrow) in the distal small bowel.

Figure 5.  Flocculation. CT image show irregular dots of barium (arrow) in fluid-filled bowel loops.

To our knowledge, there has not been a correlative study linking the histologic grade to the nodal appearance. However, lymph nodes progressively enlarge as the severity of the clinical disease increases. The degree of adenopathy is thought to correlate with the described stages, with advanced disease producing large low-attenuation or even cavitating fat-filled lymph nodes (31).

Small Bowel MABP

Although barium examination once dominated evaluation of the small bowel, its use has declined. CT is now the initial imaging modality for most nonspecific abdominal symptoms. Recognizing the CT correlates of barium abnormalities will allow the diagnosis of celiac disease to be suggested whenever abdominal CT is performed.

Scholz et al  981

Figure 4.  Dilution. CT image shows varying degrees of luminal opacification, from white to gray to fluid attenuation. This appearance is produced when opaque oral contrast material is progressively diluted as it passes into fluid-filled small bowel loops.

Advantages of CT for the diagnosis of celiac disease are simultaneous visualization of the small and large bowel, mesenteric lymph nodes, and the spleen. As with the barium MABP and with many other diseases of the small bowel seen with CT (25), not one finding but a pattern of multiple individual CT findings suggests celiac disease malabsorption. The specific CT MABP findings that may be observed in celiac disease will be illustrated. All of the individual findings (Table 1) evolve from the autoimmune attack and the resultant chronic large volumes of fluid in the small bowel. Fluid excess dilutes digestive secretions, dilates the bowel, lowers its tone, limits the mixing needed for intraluminal digestion, and delays transit, promoting secondary bacterial overgrowth in the small bowel and colon.

CT Features of Celiac Disease Small Bowel MABP Small bowel loops are often dilated and fluidfilled as a result of the chronic inflammatory process (Fig 3). This leads to progressive dilution of enteric contrast material (Fig 4). Small hyperattenuating flecks of barium may be seen precipitating in the dilated small bowel loops, a phenomenon termed flocculation (Fig 5). The small

982  July-August 2011


Figure 6.  Laminar flow. CT images (a obtained at a higher level than b) show dilated bowel loops with contrast material in the folds (arrow), then a low-attenuation layer, with a higher-attenuation layer in the lumen center. Laminar flow mimics an intussusception but lacks intramural fat.

bowel lumen contains both intrinsic physiologic fluid and administered enteric contrast material. Peristaltic waves sweeping periodically through the bowel result in variable laminar flow of these different fluid components within the flaccid bowel lumen in a recognizable pattern (Fig 6). The small bowel becomes progressively more flaccid and dilated (Fig 7). The result is telescoping of bowel loops (Fig 8) and ultimately intussusception (Fig 9), in which the mesenteric fat and vessels of one bowel loop are seen within the lumen of an adjacent bowel loop. Small bowel loops are prone to conform against each other (Fig 10), particularly in the pelvis.

Mesenteric Lymph Node Prominence Lymphadenopathy is a feature of, or response to, a variety of pathologic conditions that can be categorized into benign and malignant processes. In celiac disease and other autoimmune conditions, nodal enlargement is due to follicular hyperplasia caused by proliferation of reactive B and T lymphocytes. Chronic lymphatic stimulation is thought to be the cause of the elevated lymphoma risk in celiac disease. Prominence of upper mesenteric lymph nodes is a feature of celiac disease. Autoimmune stimulation in celiac disease provokes regional lympho-

Figure 7.  Large volume of the small bowel. CT image shows dilated bowel loops, which are not uniformly distended. In addition to the fluid-filled loops, note the dilution of contrast material and the lymph node prominence.

cytic proliferation. The duodenum and proximal jejunum are the initial organs targeted for autoimmune destruction, and nodal prominence is most marked in the upper small bowel mesentery. Mesenteric lymph node enlargement, low-attenuation lymph nodes, and cavitating lymph nodes are well-described features of celiac disease. However, cavitating or low-attenuation lymph nodes are infrequent and are found in patients with advanced symptomatic disease (31,32). Unfortunately, to our knowledge there are no recent multidetector CT criteria for what constitutes abnormal size or number of nodes in celiac

RG  •  Volume 31  Number 4

Scholz et al  983

Figure 8.  Telescoping. CT image shows concentric rings (arrow) in multiple bowel loops. The concentric rings represent bunching of folds in cross sections of flaccid loops. Although the folds collapse and crowd together, mesenteric fat and vessels are not seen in the lumen, as occurs with intussusception. There is also dilatation. Telescoping is also seen in Figure 7.

Figure 9.  Intussusception. CT image shows a crescent of mesenteric fat (arrow) containing vessels within a bowel loop, a finding typical of true small bowel intussusception. This appearance is in contrast to the telescoping in Figure 8.

Figure 11.  Lymph node prominence associated with celiac disease. CT image shows a prominent lymph node (arrow). The area of nodal tissue equaled or exceeded the area of adjacent mesenteric blood vessels on any section and in any plane. Also note the varying degrees of bowel dilatation, dilution, and conformation. Figure 10.  Conformation. CT image shows bowel loops falling together, with the walls conforming to each other without intervening space. Also note the fluid-filled loops, dilatation, and dilution. Conformation is also seen in multiple other images (eg, Figs 3 and 11).

disease. Past studies of mesenteric lymphadenopathy in other disease states and in healthy subjects did not exclude celiac disease with testing or follow-up (25,33). The recently recognized high prevalence of celiac disease makes it likely that some “healthy” subjects in past studies may have had celiac disease.

Furthermore, to our knowledge no prior studies evaluated mesenteric node size in three dimensions with reliance only on axial dimension. Rather than use of size measurements to determine prominence, lymph nodes can be considered prominent when their cumulative axial area is greater than the axial area of adjacent blood vessels (Fig 11). In severe disease, however, mesenteric hyperemia may limit the usefulness of this visual guide.

984  July-August 2011


Figure 12.  Lymph node prominence. (a) Coronal CT image shows prominent mesenteric lymph nodes (arrow) nestled against a large superior mesenteric vein and its first-degree branches. (b) CT image obtained after treatment with a gluten-free diet shows resolution of both the prominent lymph nodes and the mesenteric vein enlargement. Figure 13.  Fluid plume. CT image shows a puddle of fluid in the right colon (arrow), with air bubbles partly surrounding the plume. Air surrounding a pool of fluid in a patient with malabsorption should not be mistaken for pneumatosis. Also note the small bowel dilatation, dilution, and conformation.

Lymph nodes in celiac disease are not hyperemic, and use of intravenous contrast material readily distinguishes them from adjacent vessels that they may encircle. Nodal prominence may be subtle, with lymph nodes hiding within or adjacent to fluid-filled small bowel loops, with diluted contrast material camouflaging them. In patients with an elongated body habitus, coronal imaging may be more dramatic than axial imaging (Fig 12). In Crohn disease, nodal proliferation is noted near the diseased bowel segments, usually adjacent to the terminal ileum, the most com-

mon small bowel region affected by this disease. In mesenteric adenitis, which is seen in young adults, nodal proliferation is also most common in the terminal ileum.

RG  •  Volume 31  Number 4

Figure 14.  Large colon volume in celiac disease. CT image shows gas, fat-attenuation fluid, and solid debris filling a large colon (arrow). This pattern of distention is caused by chronic excess gas production.

Figure 16.  Encrustation of the colon wall. CT image shows a colon wall with an encrusted appearance (arrow). This appearance is the result of unemulsified fat from inadequate digestion coating the colon wall.

Colonic MABP All malabsorptive processes affect the colon. On reaching the colon, sugar and fat that are undigested by the small bowel will be “digested” by gas-producing bacteria, altering colonic function and structure. Chronic excess gas production will distend the colon, decreasing its tone and altering the appearance of both the colon and stool. Associations have been made between celiac disease

Scholz et al  985

Figure 15.  Increased colonic gas. CT image shows prominent gas throughout the colon. Increased colonic bacterial activity induced by unabsorbed nutrients will result in gas formation, filling the colon with gas and lowering the colonic tone.

and collagenous and lymphocytic colitis, owing to either chronic exposure to malabsorbed gluten and other food or to the autoimmune process directly affecting the colon (34). Individual CT features in the colon can be identified that will summate, in association with a small bowel MABP and lymph node prominence, to further indicate celiac disease. Small bowel fluid pouring into a stagnant hypotonic colon will remain in situ in the right colon, creating a cecal plume of fluid (Fig 13). A large-volume colon will be seen (Fig 14). Gas will be prominent throughout the colon (Fig 15). If sufficient fat is ingested, unemulsified fat will adhere to the colon wall like butter, giving the colon wall an encrusted appearance (Fig 16). If lung windows are used, some of the “air” will be revealed to be fat-attenuation fluid and stool, a finding indicative of steatorrhea (Fig 17). The textbook definition of steatorrhea is as follows:

986  July-August 2011


Figure 17.  Encrustation and fat-attenuation stool. (a) On a CT image obtained with a normal body window, the colon appears to be filled with gas. (b) On a CT image obtained with a lung window, what appeared to be only gas in the right colon is seen to be gas with a large volume of fat-attenuation fluid stool, a finding indicative of steatorrhea. The colon wall appears slightly thickened due to encrustation wherever the fatty stool touches the wall. Figure 18.  Geodes. CT image shows stool geodes (arrow) in the colon. These hard, rocklike aggregations of fat, fluid, and air will form in the static environment of the affected colon. They may be solitary but are often multiple throughout the colon and enhance the propensity to constipation.

“Diarrhea containing visible fat, or >7 gms of stool fat/24 hrs tested 3 days in a row (following 100 gm daily fat ingestion)” (35). However, steatorrhea is not equivalent to diarrhea, and patients may actually have constipation. A flaccid, gas-filled, low-tonicity colon will not compress and propel stool. The stool will roll and accrete fatty wall sludge, producing large geodes, round spheres of stool containing fat and air (Fig 18). With chronic distention, low tone, slow transit, and gas production, weak colon peristalsis leads to flatulence and constipation. With stasis, the geode wall may calcify due to fat saponification.

If the small bowel malabsorption is severe, large fluid volumes passed into the colon will overwhelm its absorption capacity and produce diarrhea. Instead of geode formation, a fluid-filled colon will then be seen (Fig 19). Each of the listed colonic features alone is insufficient, but in summation with small bowel changes, they should allow the diagnosis of celiac disease to be suggested. Because of this summation of small bowel, mesenteric node, and colonic appearances, CT confers a benefit over barium examination in diagnosis of celiac disease and other malabsorptive conditions.

RG  •  Volume 31  Number 4

Figure 19.  Colonic decompensation in celiac disease. CT image shows a fluid-filled colon (arrow). In late stages of celiac disease, increased volumes of fluid in the small bowel overwhelm the fluid-absorbing capacity of the colon. In conjunction with decreased tone and flaccidity, distended fluid-filled loops of colon are often seen.

Scholz et al  987

Figure 20.  Small bowel wall thickening. CT image shows prominent folds (arrow) in the small bowel, which are outlined by air and barium in the bowel lumen.

cess and reactive adenopathy, structural changes are prominent in some patients. Diseases statistically associated with but not caused by celiac disease can modulate the CT findings. Such associated diseases include insulin-dependent diabetes; psoriasis; systemic lupus erythematosus; autoimmune diseases of the liver, pancreas, and kidney; and thyroid disease.

Wall Thickening

Figure 21.  Small bowel wall thickening. CT image shows pelvic loops with wall thickening and laminar flow (top arrow) and fold prominence (bottom arrow).

Other Findings That Add Suspicion

Although the small bowel MABP and colonic MABP coupled with mesenteric node prominence strongly suggest celiac disease, the pathophysiologic features of this disease are still being unraveled. Beyond patterns induced by fluid ex-

Celiac disease has varying severity among patients as well as in each patient. The disease may be severe in the duodenum, milder in the jejunum, and minimal in the ileum. The initial phase in any segment is inflammation with fold and wall thickening. If small bowel wall thickening is observed in any segment, in conjunction with other imaging findings of celiac disease, the likelihood of celiac disease is further increased. The lymphocytic attack phases of celiac disease thicken both the jejunal folds and wall (36) (Figs 20, 21). As the inflammatory process advances in the jejunum to destructive phases 3 and 4, the attack phases progress into the ileum, thickening

988  July-August 2011


Figure 22.  Colonic wall thickening. CT images (a obtained at a higher level than b) show thickening of the colon wall (arrow).

the wall and folds; this is the basis of the reversal of folds noted long ago at barium examination. Because of the mobility of bowel loops, differentiating jejunal and ileal loops may be difficult, especially when flaccid fluid-filled loops make it difficult or impossible to trace and define the segmental location of thick folds. Jejunal loops may project into the pelvis, ileal loops into the upper abdomen. The colon wall may also become diffusely circumferentially thickened, usually becoming greater than 4 mm thick (Fig 22). The cause may be direct lymphocytic infiltration from active celiac disease. It has been shown that reflux caused by celiac disease can be treated with a gluten-free diet (37). Alternatively, colonic irritation from exposure to unabsorbed food may initiate colonic wall changes.

Other Mesenteric Manifestations The small bowel mesentery may appear hypervascular, particularly during the active inflammatory phase. Vessels may be engorged, with the superior mesenteric vein equal in diameter to the aorta (Fig 23). An edematous or “misty” mesentery has been seen, but this is a common finding in healthy patients and is still of uncertain significance.

Figure 23.  Mesenteric hypervascularity. CT image shows that the diameter of the superior mesenteric vein (arrow) is equal to that of the aorta. Small bowel inflammation in celiac disease results in high vascular flow through the small bowel.

Intramural Fat Intramural fat can be seen in the duodenal and jejunal wall in patients with celiac disease (38) (Fig 24). Intramural fat has also been observed in the wall of the right colon (Fig 25). As with intramural fat in the distal small bowel in Crohn disease, intramural fat in celiac disease is believed to be the result of chronic inflammatory processes stimulating fat deposition.

RG  •  Volume 31  Number 4

Scholz et al  989

Figures 24, 25.  (24) Small bowel intramural fat. CT images show intramural fat in the duodenum (arrow in a) and jejunum (arrow in b). (25) Colonic intramural fat. CT image shows intramural fat in the right colon (arrow). If intramural fat is noted in the large bowel, it may be a feature of celiac disease, a feature of associated collagenous or lymphocytic colitis, or a colonic response to malabsorption.

Figure 26.  Cavitary mesenteric lymph node syndrome. (a) CT image shows splenic atrophy. The spleen (arrow) is smaller than the kidney. (b) CT image shows mesenteric lymph nodes of fluid attenuation (28 HU).

Splenic Atrophy and Cavitary Mesenteric Lymph Node Syndrome Splenic atrophy may occur in celiac disease (Fig 26a). Rarely, it may be part of a trio of findings in advanced disease called the cavitary lymph node

syndrome (Fig 26b) (31,32). This syndrome consists of a small or dysfunctional spleen, low-attenuation lymph nodes, and severe villous atrophy.

990  July-August 2011


Table 2 Other Causes of the MABP General Causes

Specific Causes and Examples

Abnormal digestion   Low levels of digestive juices   High levels of digestive juices   Bowel diseases   Short small bowel   Long small bowel Abnormal ingestion   High fat intake   Cathartics and nonabsorbable sugars

Pancreatic, hepatic, and biliary insufficiency Zollinger-Ellison syndrome–associated gastrinoma, VIPoma Lactose intolerance, Crohn disease, tropical sprue, chronic ischemia Resection, bypass, Roux-en-Y anastomosis (eg, Billroth II anastomosis) Dysmotility disease, narcotics, hypothyroidism, psychotropics, radiation therapy, chemotherapy Binge eating, enteric tube feeding Miralax,* sorbitol, lactulose, mannitol, maltitol

*Polyethylene glycol 3350 (Merck/Schering Plough Pharmaceuticals, North Wales, Penn).


Celiac disease is now recognized as a common condition with significant long-term morbidity and increased risk of mortality. It is likely to be the commonest disease of the small bowel. However, most cases remain undiagnosed. This is in part due to the relatively low and nonspecific morbidity during the early disease course, with chronic mild pain and anemia. CT is commonly performed for these reasons as well as for many other abdominal symptoms. Early recognition and treatment virtually eliminate the morbidity of celiac disease and the risk of mortality. Treatment with a gluten-free diet has been shown to produce interval resolution of hypervascularity, dilatation, dilution, and conformation (Fig 27). A pattern of small bowel and colonic findings with mesenteric lymph node prominence at CT should suggest the diagnosis of celiac disease. A simple blood test costing less than $100 usually allows confirmation of the diagnosis (11,39). A negative test result may not allow exclusion of celiac disease in a few patients with immunoglobulin A deficiency or with severe disease creating an inability to mount an antibody response. Celiac disease is highly prevalent and is probably the single most common disease causing the MABP at CT. Knowledge of the pathophysiologic mechanisms of celiac disease helps one comprehend the spectrum of imaging findings.

However, many other pathologic processes may cause the MABP (Table 2). Understanding the digestive process is essential for understanding the CT findings in celiac disease and other bowel diseases associated with malabsorption (40). In all patients with the MABP, review of the clinical history, examination results, and laboratory findings should be used in concert with CT to diagnose celiac disease or other MABP-associated diseases. Recognition of the MABP at CT should encourage further clinical testing and evaluation (Fig 28). Celiac disease will remain a difficult disease for radiologists to confidently diagnose. Pathologic correlation is limited to duodenal biopsy. There is great variability in the severity of clinical disease, which likely causes a similar spectrum of CT findings. Correlation of imaging findings with disease status is difficult. Long prodromal periods with a wide variety of symptoms are typical. Additional study of celiac disease is needed to establish a relationship between disease severity and CT findings. Further understanding of celiac disease is required to establish the effects of diet and comorbid conditions on the MABP. Since diet and digestion are highly variable and affect the appearance of the bowel, a large blinded comparison of celiac disease patients with matched healthy control patients would be useful. Determination of the sensitivity and specificity of individual features of the MABP for celiac disease might be helpful in distinguishing celiac disease from other causes of malabsorption.

RG  •  Volume 31  Number 4

Scholz et al  991

Figure 27.  Treatment of celiac disease. CT images, obtained before (a) and 1 year after (b) treatment with a gluten-free diet, show interval resolution of hypervascularity, dilatation, dilution, and conformation (arrow).

Figure 28.  Advanced untreated celiac disease. CT images (displayed from superior [top left] to inferior [bottom right]) show the following findings: absent body fat; ascites; steatohepatitis with compressed hepatic veins and a triangular inferior vena cava; a small-volume spleen; the small bowel MABP with dilution, dilatation, and flocculation; mesenteric lymph nodes obscured amid small bowel loops; and prominent fluid and gas in the colon.

References 1. Rubio-Tapia A, Kyle RA, Kaplan EL, et al. Increased prevalence and mortality in undiagnosed celiac disease. Gastroenterology 2009;137(1):88–93. 2. Catassi C, Kryszak D, Louis-Jacques O, et al. Detection of celiac disease in primary care: a multicenter case-finding study in North America. Am J Gastroenterol 2007;102(7):1454–1460. 3. Marsh MN. Gluten, major histocompatibility complex, and the small intestine: a molecular and immunobiologic approach to the spectrum of gluten sensitivity (‘celiac sprue’). Gastroenterology 1992;102 (1):330–354. 4. Green PH, Cellier C. Celiac disease. N Engl J Med 2007;357(17):1731–1743.

5. Herlinger H. Radiology in malabsorption. Clin Radiol 1992;45(2):73–78. 6. Marshak RH, Wolf BS, Adlersberg D. Roentgen studies of the small intestine in sprue. Am J Roentgenol Radium Ther Nucl Med 1954;72(3):380–400. 7. Jones S, D’Souza C, Haboubi NY. Patterns of clinical presentation of adult coeliac disease in a rural setting. Nutr J 2006;5:24. 8. Bova JG, Friedman AC, Weser E, Hopens TA, Wytock DH. Adaptation of the ileum in nontropical sprue: reversal of the jejunoileal fold pattern. AJR Am J Roentgenol 1985;144(2):299–302.

992  July-August 2011 9. Tully TE, Feinberg SB. A roentgenographic classification of diffuse diseases of the small intestine presenting with malabsorption. Am J Roentgenol Radium Ther Nucl Med 1974;121(2):283–290. 10. Herlinger H. Guide to imaging of the small bowel. Gastroenterol Clin North Am 1995;24(2):309–329. 11. van der Windt DA, Jellema P, Mulder CJ, Kneepkens CM, van der Horst HE. Diagnostic testing for celiac disease among patients with abdominal symptoms: a systematic review. JAMA 2010;303(17): 1738–1746. 12. Soyer P, Boudiaf M, Fargeaudou Y, et al. Celiac disease in adults: evaluation with MDCT enteroclysis. AJR Am J Roentgenol 2008;191(5):1483–1492. 13. Sanders DS, Hopper AD, Azmy IA, et al. Association of adult celiac disease with surgical abdominal pain: a case-control study in patients referred to secondary care. Ann Surg 2005;242(2):201–207. 14. Jafri MR, Nordstrom CW, Murray JA, et al. Longterm fracture risk in patients with celiac disease: a population-based study in Olmsted County, Minnesota. Dig Dis Sci 2008;53(4):964–971. 15. Khashan AS, Henriksen TB, Mortensen PB, et al. The impact of maternal celiac disease on birthweight and preterm birth: a Danish population-based cohort study. Hum Reprod 2010;25(2):528–534. 16. Ludvigsson JF, Montgomery SM, Ekbom A, Brandt L, Granath F. Small-intestinal histopathology and mortality risk in celiac disease. JAMA 2009;302(11): 1171–1178. 17. Scholz FJ, Behr SC, Scheirey CD. Intramural fat in the duodenum and proximal small intestine in patients with celiac disease. AJR Am J Roentgenol 2007;189(4):786–790. 18. Moser PP, Smith JK. CT findings of increased splanchnic circulation in a case of celiac sprue. Abdom Imaging 2004;29(1):15–17. 19. Reddy D, Salomon C, Demos TC, Cosar E. Mesenteric lymph node cavitation in celiac disease. AJR Am J Roentgenol 2002;178(1):247. 20. Jones B, Bayless TM, Fishman EK, Siegelman SS. Lymphadenopathy in celiac disease: computed tomographic observations. AJR Am J Roentgenol 1984;142(6):1127–1132. 21. Soyer P, Boudiaf M, Dray X, et al. CT enteroclysis features of uncomplicated celiac disease: retrospective analysis of 44 patients. Radiology 2009;253(2): 416–424. 22. Horton KM, Fishman EK. Uncommon inflammatory diseases of the small bowel: CT findings. AJR Am J Roentgenol 1998;170(2):385–388. 23. Tomei E, Marini M, Messineo D, et al. Computed tomography of the small bowel in adult celiac disease: the jejunoileal fold pattern reversal. Eur Radiol 2000;10(1):119–122.

radiographics.rsna.org 24. Paolantonio P, Tomei E, Rengo M, Ferrari R, Lucchesi P, Laghi A. Adult celiac disease: MRI findings. Abdom Imaging 2007;32(4):433–440. 25. Macari M, Megibow AJ, Balthazar EJ. A pattern approach to the abnormal small bowel: observations at MDCT and CT enterography. AJR Am J Roentgenol 2007;188(5):1344–1355. 26. Fasano A, Berti I, Gerarduzzi T, et al. Prevalence of celiac disease in at-risk and not-at-risk groups in the United States: a large multicenter study. Arch Intern Med 2003;163(3):286–292. 27. Schuppan D, Dennis MD, Kelly CP. Celiac disease: epidemiology, pathogenesis, diagnosis, and nutritional management. Nutr Clin Care 2005;8(2): 54–69. 28. Dickey W, Kearney N. Overweight in celiac disease: prevalence, clinical characteristics, and effect of a gluten-free diet. Am J Gastroenterol 2006;101(10): 2356–2359. 29. Fine KD. The prevalence of occult gastrointestinal bleeding in celiac sprue. N Engl J Med 1996;334 (18):1163–1167. 30. Martel J, Sussman DA, Goldberg RI, Valantas M, Barkin JS. Benign small bowel thickening and lymphadenopathy: a manifestation of celiac disease. Dig Dis Sci 2009;54(4):902–905. 31. Matuchansky C, Colin R, Hemet J, et al. Cavitation of mesenteric lymph nodes, splenic atrophy, and a flat small intestinal mucosa: report of six cases. Gastroenterology 1984;87(3):606–614. 32. Schmitz F, Herzig KH, Stüber E, et al. On the pathogenesis and clinical course of mesenteric lymph node cavitation and hyposplenism in coeliac disease. Int J Colorectal Dis 2002;17(3):192–198. 33. Lucey BC, Stuhlfaut JW, Soto JA. Mesenteric lymph nodes seen at imaging: causes and significance. RadioGraphics 2005;25(2):351–365. 34. Freeman HJ. Update on collagenous sprue. World J Gastroenterol 2010;16(3):296–298. 35. Schiller LR, Sellin JH. Diarrhea. In: Feldman M, Friedman LS, Brandt LJ, eds. Sleisenger and Fordtran’s gastrointestinal and liver disease: pathophysiology/diagnosis/management. 8th ed. Philadelphia, Pa: Saunders Elsevier, 2006; 159–186. 36. Farrell RJ, Kelly CP. Celiac sprue. N Engl J Med 2002;346(3):180–188. 37. Nachman F, Vázquez H, González A, et al. Gastroesophageal reflux symptoms in patients with celiac disease and the effects of a gluten-free diet. Clin Gastroenterol Hepatol 2011;9(3):214–219. 38. Tully MA. Pediatric celiac disease. Gastroenterol Nurs 2008;31(2):132–140. 39. Hill ID. What are the sensitivity and specificity of serologic tests for celiac disease? Do sensitivity and specificity vary in different populations? Gastroenterology 2005;128(4 suppl 1):S25–S32. 40. Rubesin SE, Herlinger H, Furth EE. “Bubbly” duodenal bulb in clinically unsuspected or refractory adult celiac disease. Abdom Imaging 1998;23(4): 449–452.


This journal-based CME activity has been approved for AMA PRA Category 1 Credit . See www.rsna.org/education/rg_cme.html.

Teaching Points

July-August Issue 2011

CT Findings in Adult Celiac Disease Francis J. Scholz, MD • Jalil Afnan, MD • Spencer C. Behr, MD RadioGraphics 2011; 31:977–992 • Published online 10.1148/rg.314105215 • Content Codes:

Page 978 (Figure on page 979) Features of the celiac disease MABP include duodenitis (7) (Fig 1a), dilution, dilatation, slow transit, flocculation (Fig 1b), moulage (Fig 1c), reversal of the jejunal-ileal fold pattern (8) (Fig 1d), and transient small bowel intussusception. Page 978 The celiac disease pattern has several components: the small bowel MABP, mesenteric lymph node prominence in the small bowel, and the colonic MABP. Page 978 Once thought to be a relatively rare diarrhea-associated debilitating disease affecting 1 in 10,000–30,000 individuals, primarily children, celiac disease is now estimated to occur in 1 in 200 Americans of any age (26). Page 983 (Figure on page 983) Rather than use of size measurements to determine prominence, lymph nodes can be considered prominent when their cumulative axial area is greater than the axial area of adjacent blood vessels (Fig 11). Page 990 Early recognition and treatment virtually eliminate the morbidity of celiac disease and the risk of mortality.