DOI: 10.1148/rg.283065179
RadioGraphics 2008;28:727-746
© RSNA, 2008
Bowel Wall Thickening in Children: CT Findings1
Maria d’Almeida, MD,
Jean Jose, DO,
Julieta Oneto, MD, and
Ricardo Restrepo, MD
1 From the Department of Radiology, Miami Children’s Hospital, 3100 SW 62nd Ave, Miami, FL 33155. Presented as an education exhibit at the 2005 RSNA Annual Meeting. Received October 9, 2006; revision requested November 9 and received August 20, 2007; accepted November 9. All authors have no financial relationships to disclose.
Address correspondence to R.R. (e-mail: Ricardo.Restrepo{at}mch.com).
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Abstract
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A wide variety of bowel diseases, some of which are unique to or more prevalent in pediatric patients, may manifest with intestinal wall thickening at computed tomography (CT). Common causes of bowel wall thickening include edema, hemorrhage, infection, graft-versus-host disease, and inflammatory bowel disease; more unusual causes include immunodeficiencies, lymphoma, hemangioma, pseudotumor, and Langerhans cell histiocytosis. Radiologists must be familiar with the CT signs of bowel disease and should take careful note of the bowel characteristics (eg, extent and distribution of disease involvement, bowel dilatation, mural stratification, perienteric findings) to generate an adequate differential diagnosis. The study should be tailored and optimized in advance according to the clinical scenario to decrease radiation exposure due to repeated or delayed scanning. With spiral CT scanners, studies can be performed quickly, thereby eliminating the need for sedation, and multiple reconstructed images can be generated. CT is an invaluable diagnostic tool in the evaluation of pediatric diseases involving the bowel, in spite of the use of ionizing radiation.
© RSNA, 2008
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Introduction
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There is a considerable amount of literature on the computed tomographic (CT) evaluation of the bowel in adults but very little on bowel CT in children. 
The differential diagnosis for diseases affecting the bowel in pediatric patients can be narrowed by paying attention to specific radiologic signs and the patient’s clinical history. Certain diseases affect the small and large bowel simultaneously.
CT is an increasingly useful technique in the evaluation of intestinal disease, allowing the evaluation of bowel disease as well as extraintestinal disease. CT also provides an excellent assessment of the perienteric abnormalities that frequently accompany bowel disease (eg, adenopathy, ascites, fat stranding, presence of abscesses and fistulas) and improves specificity in diagnosis (1). In this article, we review CT technique in the evaluation of bowel disease in pediatric patients. We also discuss and illustrate the CT appearances of various bowel diseases in these patients in terms of cause of disease (infection, trauma, neoplasm, inflammation, autoimmune causes, mechanical causes) as well as extent and distribution of involvement.
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Technical Considerations
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The faster scanning times made possible by multidetector (spiral) technology decrease the need for sedation in children. At our institution, we currently use a 16-detector CT scanner. We obtain 5-mm-thick axial images that are routinely retrospectively reformatted in the coronal plane. If the patient is less than 6 months old, we obtain 3.75-mm-thick axial images. Extra efforts are required to decrease the radiation exposure related to repetitive scanning by optimizing bowel preparation and imaging parameters. All images are acquired after the oral and intravenous administration of contrast material, with no routine acquisition of delayed images. If sedation is required, oral contrast material is administered approximately 15–20 minutes before placing the child on the CT table. This 15–20-minute period, plus the time required to sedate the child, accounts for the 40–45 minutes just prior to the actual scanning. When sedation is not required, patients are scanned 1 hour after the ingestion of oral contrast material.
Children’s reluctance to drink oral contrast material and their decreased mesenteric fat makes the examination more challenging. At our institution, iohexol (Omnipaque; Nycomed Amersham, Princeton, NJ) mixed with Gatorade (Quaker Oats, Chicago, Ill) is offered initially to children. Besides being nonionic, iohexol is tasteless and has a thinner consistency, increasing patient compliance. In addition, we have noticed a faster transit time, yielding better enhancement of more distal portions of the colon and sometimes even of the rectum. When there is a history of iodine allergy, the child is offered flavored barium suspension. We also use cold water as a negative contrast agent more frequently in children who refuse other oral contrast agents and when the evaluation of the mucosa is most important, such as in graft-versus-host disease (GVHD) and vasculitis. Cold water is better tolerated when nausea is present; however, it makes the timing of the study more challenging because of its rapid absorption through the bowel and the lack of colonic distention. In addition, water makes the wall of the bowel more conspicuous and may give the false impression of mild thickening (Fig 1).
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Figure 1. CT scan obtained with intravenous contrast material and with water as a negative oral contrast agent gives a false impression of mild wall thickening of the jejunum (arrow).
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Although not available at our institution, Volumen (0.1% barium suspension) (E-Z-EM, Westbury, NY) can be used as well. This negative contrast agent is an alternative to water, with the benefits of a faster transit time and no bowel absorption.
In our opinion, the use of a negative contrast agent has few disadvantages. Such agents limit the examination when fistulous tracts or intramural accumulation of contrast material is present. In cases of acute appendicitis, filling of the appendix and surrounding bowel loops with negative oral contrast material could potentially confuse the picture. An appendix filled with a positive contrast agent is easier to recognize and virtually excludes appendicitis.
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Normal Bowel
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Knowledge of the histologic structure of the bowel wall will facilitate understanding of the pathophysiologic findings, since specific entities may affect certain layers or the entire wall thickness (Figs 2–4).
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Figure 4. Drawing illustrates the normal colon. A = cecum, B = ascending colon, C = haustra, D = transverse colon, E = epiploic appendages, F = free tenia, G = descending colon, H = sigmoid colon.
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Bowel Characterization
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Adequate and complete characterization of the bowel with use of an algorithmic approach will generate a reasonable differential diagnosis and, in some cases, lead to a specific diagnosis. Several findings should be taken into account when characterizing the wall of the bowel, but recognizing the presence and degree of bowel wall thickening (Fig 5) is of the utmost importance. Some authors have described the normal bowel wall thickness in adults as 1–2 mm when the lumen is distended. Colonic wall thickness is more dependent on distention and intraluminal contents than is small bowel wall thickness. When distended, the colonic wall is often imperceptible (Fig 6) (2,3). To our knowledge, there are no published standards of normal bowel wall thickness in children. As a practical general rule, the bowel wall should be barely perceptible when adequately distended.
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Figure 6a. (a) CT scan obtained with oral and intravenous contrast material shows poor distention of the cecum (arrow), a finding that simulates bowel wall thickening. There is evidence of seat belt injury in the anterior abdominal wall. (b) Delayed CT scan obtained with oral contrast material shows adequate distention of the cecum (arrow) and no cecal wall thickening.
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Figure 6b. (a) CT scan obtained with oral and intravenous contrast material shows poor distention of the cecum (arrow), a finding that simulates bowel wall thickening. There is evidence of seat belt injury in the anterior abdominal wall. (b) Delayed CT scan obtained with oral contrast material shows adequate distention of the cecum (arrow) and no cecal wall thickening.
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When a peristaltic loop is imaged, transient wall thickening is present, usually posing no diagnostic dilemma at CT. Depending on the degree of bowel wall thickening, luminal narrowing may lead to proximal bowel dilatation. Pseudomembranous colitis and Crohn disease tend to be associated with the most severe wall thickening (4).
Distribution of the wall thickening is a critical finding, since several diseases follow a well-established pattern and others affect either the small bowel, the large bowel, or both. The distribution may be focal (only a few centimeters), segmental (usually a few bowel loops), diffuse (either the entire small bowel or large bowel), or universal (the entire small and large bowel).
Some diseases demonstrate a specific pattern of wall thickening. Eccentric involvement is more commonly seen with tumors, either benign or malignant, whereas circumferential thickening tends to occur with inflammatory conditions and infections. One exception to this rule is the "apple core" sign, which represents luminal narrowing resulting from focal circumferential wall thickening of the bowel. This sign is most commonly but not exclusively associated with colonic adenocarcinoma.
Several patterns of wall attenuation have been described in association with specific diseases. A hyperattenuating wall is seen with hemorrhage as a result of trauma, purpura, or vasculitis. A submucosal fatty "halo" (Fig 7) has been described as a result of chronic inflammation, such as in inflammatory bowel disease and GVHD. A fatty halo has also been reported in asymptomatic obese patients (5). The term pneumatosis refers to air in the bowel wall. Intramural gas may have a different appearance, depending on whether it is submucosal or subserosal; the former is bubbly or cystic in appearance and the latter is curvilinear. Pneumatosis is an imaging finding and not a diagnosis (Fig 8). It should be considered a sign of acute injury, although on occasion it has been associated with chronic preexisting conditions. More than 50 causes have been identified, from ischemia to nonemergent medical and iatrogenic causes. In addition to ischemia, pneumatosis in children has been associated with rotavirus gastroenteritis, bowel obstruction such as pyloric stenosis and meconium ileus, accidental and nonaccidental trauma, steroids, chemotherapy, and organ transplantation. Cystic fibrosis and asthma may also result in pneumatosis (6–8). A significant number of cases have underlying risk factors, most commonly related to immunosuppression.
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Figure 7. Fatty halo in a patient with long-standing ulcerative colitis. CT scan obtained with oral contrast material shows low-attenuation areas in the colonic wall (arrow), findings that represent fat deposits in the submucosal layer.
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Figure 8. Pneumatosis in a patient with a history of bone marrow transplantation who was receiving steroids. CT scan (bone window) demonstrates linear subserosal mural air (arrows).
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Submucosal edema is definitive evidence of bowel wall injury (typically acute), often producing the "target" sign (Fig 9). Mural stratification is due to hypoattenuating submucosal edema, with the enhancing hyperattenuating inner and outer layers of the target representing the mucosa and muscularis propria–serosa, respectively (9).
Other CT signs have been associated with specific disease entities in the literature. The "accordion" sign is caused by contrast material trapped between thickened edematous haustral folds in the colon (Fig 10). Although the accordion sign is most commonly seen in pseudomembranous colitis, it is not pathognomonic for this disease (10). The "comb" sign represents hypervascular engorged vasa recta aligned like the teeth of a comb on the mesenteric site of the bowel (Fig 11). This finding is classically seen in inflammatory bowel disease, especially Crohn disease, and suggests a clinically active disease. The comb sign can also be seen in vasculitis and purpura (11). The "toothpaste" or "lead pipe" sign has been associated with chronic diseases leading to a "featureless" bowel (Fig 12). It is commonly seen with Crohn disease or chronic GVHD or as the sequela of radiation therapy.
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Figure 12a. Toothpaste sign in a patient with chronic GVHD. (a) CT scan obtained with oral and intravenous contrast material shows diffuse concentric small bowel wall thickening (arrow). Mural stratification (arrowhead) and narrowing of the descending colon are also noted. (b) Delayed image from a small bowel follow-through examination shows diffuse narrowing of the descending colon (arrow), a finding that is the result of chronic GVHD.
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Figure 12b. Toothpaste sign in a patient with chronic GVHD. (a) CT scan obtained with oral and intravenous contrast material shows diffuse concentric small bowel wall thickening (arrow). Mural stratification (arrowhead) and narrowing of the descending colon are also noted. (b) Delayed image from a small bowel follow-through examination shows diffuse narrowing of the descending colon (arrow), a finding that is the result of chronic GVHD.
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Bowel Diseases
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Infection
The bowel may be affected by a large number of infectious agents. Gastroenteritis and colitis are probably the most common causes of bowel wall thickening and are usually diagnosed clinically. Occasionally, however, they are identified at CT, either incidentally or as an atypical manifestation. It is difficult to make the diagnosis of a specific type of infection on the basis of imaging findings alone, with laboratory analysis usually being required. Some bacterial causes include Escherichia coli, Shigella, Salmonella, Yersinia, Campylobacter, and Staphylococcus. Viral causes include Rotavirus, Herpes, and Cytomegalovirus. Rotavirus is a very common cause of gastroenteritis in infants and children. It most often affects children between 6 months and 2 years of age during the winter months. Parasitic infections such as amebiasis are more common in underdeveloped countries.
The segment of the colon involved may suggest a specific diagnosis. Most of the bacterial colitides tend to involve the right colon. Certain ancillary signs such as lymphadenopathy and splenomegaly suggest Salmonella. Diffuse involvement suggests E coli or Cytomegalovirus. The rectosigmoid colon tends to be involved with Herpes, Neisseria gonorrhoeae , and Treponema pallidum as part of the so-called gay bowel syndrome (Fig 13). This syndrome was first described in the 1980s in adolescents and is often unfamiliar to pediatricians but should be considered in the differential diagnosis for a homosexual adolescent with abdominal pain. The patient’s sexual history is critical in suggesting the diagnosis (12).
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Figure 13. Gay bowel syndrome in a homosexual teenager. CT scan obtained with oral and intravenous contrast material shows segmental wall thickening of the sigmoid colon (arrow). Herpes simplex infection was confirmed at biopsy.
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Of the bacterial infections, two entities deserve particular attention with respect to their occurrence in children: pseudomembranous colitis and E coli infection.
Pseudomembranous Colitis.—
Pseudomembranous colitis results from toxins produced by an overgrowth of Clostridium difficile , most often but not exclusively associated with antibiotic therapy. The use of any antibiotic, most commonly clindamycin, may result in pseudomembranous colitis. CT findings include extreme segmental or diffuse wall thickening, either confined to a segment or involving the entire colon (Fig 14). The degree of wall thickening is greater than in any other infectious or inflammatory process involving the bowel except for Crohn disease (13). The so-called accordion sign is suggestive of but not pathognomonic for this entity and is usually seen in advanced cases (10). Typically, no significant pericolonic fat stranding is seen.
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Figure 14. Pseudomembranous colitis in a patient with proved C difficile colitis. CT scan obtained with oral and intravenous contrast material shows severe colonic wall thickening with trapped oral contrast material between edematous haustral folds (arrow).
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E coli Infection.—
Unlike in adults, E coli infection in children may result in hemolytic uremic syndrome. This syndrome is triggered by an infection that induces an autoimmune response characterized by a microangiopathic hemolytic anemia, thrombocytopenia, and renal failure. E coli is the most commonly isolated micro-organism. E coli infection occurs predominantly in infants and young children and is the most common cause of acute renal failure in children. The cecum and ascending colon are the most commonly involved areas. CT findings include mural stratification, narrowing of the bowel lumen, and pericolonic fat stranding (Fig 15). Colonic ischemia and perforation are well-known complications.
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Figure 15a. Hemolytic uremic syndrome from E coli infection (proved at culture) in a pediatric patient. (a) Coronal CT scan obtained with oral and intravenous contrast material shows diffuse concentric colonic wall thickening (arrows). (b) Sagittal ultrasonographic (US) image of the hepatorenal fossa demonstrates a diffusely enlarged and echogenic right kidney, a finding that indicates medicorenal disease.
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Figure 15b. Hemolytic uremic syndrome from E coli infection (proved at culture) in a pediatric patient. (a) Coronal CT scan obtained with oral and intravenous contrast material shows diffuse concentric colonic wall thickening (arrows). (b) Sagittal ultrasonographic (US) image of the hepatorenal fossa demonstrates a diffusely enlarged and echogenic right kidney, a finding that indicates medicorenal disease.
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Trauma
In pediatric patients, target organs and resulting injuries after abdominal trauma are somewhat different than in adults. The mechanism of trauma (nonaccidental trauma, handle bar injury, back seat location in motor vehicle accidents) accounts for some of the differences. The duodenum and small bowel are commonly injured after trauma. Typically, duodenal hematomas are intramural, involving the second or third portion of the duodenum (Fig 16). The characteristic finding is an eccentric mass protruding into the bowel lumen and causing varying degrees of obstruction. The attenuation of the mass varies according to the time of trauma; in acute trauma, the mass tends to be slightly hyperattenuating. In focal or segmental small bowel hematomas, more pronounced and localized enhancing wall thickening is usually present (Fig 17). A careful search for signs of perforation, mesenteric and abdominal wall hematomas, and spinal fractures must be performed.
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Figure 16. Duodenal hematoma. CT scan obtained with oral and intravenous contrast material shows marked focal duodenal wall thickening (arrow). Free fluid and fat stranding are seen in the right paracolic gutter (arrowhead) and anterior abdomen.
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Figure 17. Jejunal hematoma. CT scan obtained with oral and intravenous contrast material shows diffuse concentric jejunal wall thickening with associated abnormal enhancement (arrowhead) and hemoperitoneum (curved arrow). Straight arrow indicates periumbilical fat stranding of the anterior abdominal wall, a finding that is due to seat belt injury.
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Hypoperfusion complex–shock bowel syndrome is the manifestation of a tenuous hemodynamic instability, usually secondary to trauma even after aggressive resuscitation efforts with intravenous fluid. It is seen predominantly in infants and young children. CT findings include dilated and fluid-filled small bowel loops with sparing of the colon. The small bowel wall is thickened in a diffuse and concentric fashion, displaying intense enhancement after contrast material administration (Fig 18). In more severe cases, an abnormal intense parenchymal enhancement of solid organs such as the kidneys and adrenal glands, a small-caliber aorta, and a collapsed inferior vena cava are present (14,15).
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Figure 18. Hypoperfusion complex in a patient with a history of trauma. CT scan obtained with oral and intravenous contrast material shows hyperattenuating diffuse small bowel wall thickening (arrowhead), a small-caliber aorta, and a collapsed inferior vena cava (straight arrows). Hemoperitoneum (curved arrows) and renal contusions are also present.
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Neoplasm
Tumors may arise from any of the components of the bowel wall: the mucosa, muscular layer, nerves, lymphoid tissue, or vessels.
Lymphoma.—
Lymphoma is a common neoplasm of childhood. Primary gastrointestinal lymphoma is most frequently of B-cell origin, predominantly of the non-Hodgkin type. Secondary bowel involvement from generalized lymphomas is more common than primary lymphoma. The appearances of T-cell lymphomas of the bowel include plaques, mucosal ulceration, and strictures, whereas B-cell type lymphoma manifests as polypoid masses (Fig 19) or eccentric wall thickening. Aneurysmal dilatation secondary to destruction of the autonomic nerve plexus by tumor infiltration can be seen. The presence of hepatosplenomegaly and hypoattenuating bulky adenopathy are supporting findings. Both the small bowel and colon are involved; however, B-cell lymphomas tend to affect the distal ileum, whereas T-cell types affect the duodenum and jejunum.
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Figure 19. Lymphoma. Contrast material–enhanced CT scan shows two small bowel intussusceptions (arrowheads). The right-sided intussusception contains mesenteric fat (arrow), which is not an unusual manifestation of lymphoma.
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Gastrointestinal Stromal Tumors.—
Gastrointestinal stromal tumors are the most common mesenchymal neoplasms of the gastrointestinal tract. The most common site of involvement is the stomach, followed by the small intestine, anorectum, colon, and esophagus. Gastrointestinal bleeding due to mucosal ulceration is usually the presenting sign. These tumors arise from the muscularis propria, typically manifesting as an eccentric well-circumscribed mass, occasionally with a hypoattenuating center representing cystic degeneration or necrosis (Fig 20) (16).
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Figure 20a. Gastrointestinal stromal tumor. Consecutive CT scans obtained with oral and intravenous contrast material show a large, low-attenuation eccentric mass with intense peripheral enhancement (arrow) arising from the second portion of the duodenum.
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Figure 20b. Gastrointestinal stromal tumor. Consecutive CT scans obtained with oral and intravenous contrast material show a large, low-attenuation eccentric mass with intense peripheral enhancement (arrow) arising from the second portion of the duodenum.
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Neurogenic Tumors.—
One example of a neurogenic tumor is a mesenteric plexiform neurofibroma associated with neurofibromatosis. Mesenteric neurofibromas are very rare but should be suspected if a mesenteric mass is seen with or without wall thickening of the small or large bowel in a patient with neurofibromatosis (Fig 21). The diagnosis is usually suggested when multiple neurofibromas are identified elsewhere in the body.
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Figure 21. Mesenteric neurofibroma in a patient with neurofibromatosis type I. CT scan obtained with oral and intravenous contrast material shows moderate concentric cecal wall thickening (arrowhead), with an adjacent lobulated soft-tissue mass (arrow) that represents a mesenteric neurofibroma.
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Vascular Tumors.—
Although hemangiomas are common vascular tumors occurring anywhere in the body, they seldom involve the gastrointestinal tract. Most hemangiomas are pedunculated, intraluminal polypoid lesions; occasionally, they may have an infiltrative growth pattern. If there is diffuse involvement, the term hemangiomatosis should be used. The small bowel is the most commonly affected site, with jejunal predominance. CT findings include diffuse infiltration of the intestinal wall with mural thickening and occasional phleboliths. A hyperattenuating, markedly enhancing bowel wall is a classic finding (Fig 22) that is better seen when a negative oral contrast agent such as water is used (17).
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Figure 22. Hemangiomatosis. Coronal CT scan obtained with negative oral and intravenous contrast material shows intense enhancement and moderate thickening (arrow) of small bowel loops.
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Colon Cancer.—
Arising from the mucosa, adenocarcinoma of the colon is rare in the pediatric age group but can occasionally manifest in the 2nd decade of life. The transverse colon and the rectosigmoid are the two most commonly affected sites. The low 5-year survival rate is related to the nonspecific presenting complaints and the large percentage of undifferentiated types. Children with a family history of colon cancer, chronic ulcerative colitis, or familial polyposis syndromes are at greater risk. Imaging findings do not differ from those encountered in the adult population, with radiologic features including polypoid, ulcerative, annular constricting (apple core sign) (Fig 23), and scirrhous carcinomas. The complications of colon cancer include bowel obstruction, intussusception (polypoid lesions), perforation, local recurrence, and peritoneal spread (18).
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Figure 23a. Colonic adenocarcinoma. (a) CT scan obtained with oral and intravenous contrast material shows concentric segmental wall thickening of the sigmoid colon (arrow) producing significant narrowing of the lumen. (b) Image from a barium enema examination shows a stricture of the sigmoid colon (arrow) with overhanging edges (arrowhead), findings that produce an "apple core" appearance and correspond to the findings seen at CT.
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Figure 23b. Colonic adenocarcinoma. (a) CT scan obtained with oral and intravenous contrast material shows concentric segmental wall thickening of the sigmoid colon (arrow) producing significant narrowing of the lumen. (b) Image from a barium enema examination shows a stricture of the sigmoid colon (arrow) with overhanging edges (arrowhead), findings that produce an "apple core" appearance and correspond to the findings seen at CT.
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Langerhans Cell Histiocytosis.—
Involvement of the gastrointestinal tract in Langerhans cell histiocytosis may be part of a generalized disease or, rarely, a separate primary entity. Within the small bowel, Langerhans cell histiocytosis most commonly affects the terminal ileum, producing diarrhea, protein-losing enteropathy, and malabsorption (Fig 24). Colonic involvement has also been reported (19). Other causes of small bowel wall thickening related to malabsorption syndromes include celiac disease and lactose intolerance. In addition, hypoproteinemia may be seen involving the wall of the gastrointestinal tract, most commonly the small bowel. Hypoproteinemia causes diffuse, hypoattenuating wall thickening with prominence of the folds (Fig 25) and, in more severe cases, ascites. In children, it is commonly seen in nephrotic syndrome and renal failure from various causes.
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Figure 24. Langerhans cell histiocytosis. CT scan obtained with oral and intravenous contrast material shows diffuse concentric jejunal wall thickening (arrow) causing luminal narrowing (arrowhead).
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Figure 25. Hypoproteinemia in a patient with chronic renal failure. CT scan obtained with oral and intravenous contrast material shows concentric wall thickening of the jejunum (arrow). Multiple cysts are incidentally seen in the atrophic right kidney (arrowhead).
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Inflammation
Inflammatory Bowel Disease.—
Crohn disease and ulcerative colitis are very important and relatively common causes of bowel wall thickening in children. Approximately 25% of cases of Crohn disease and 20% of cases of ulcerative colitis occur in children (20); earlier onset tends to occur in patients with a family history of the disease. Ulcerative colitis usually starts during adolescence. Much overlap exists in the imaging - characteristics of these two diseases, and the major imaging features are similar to those in adults. Crohn disease more frequently involves the terminal ileum and the right colon (Fig 26), whereas exclusive right colonic involvement is rare in ulcerative colitis. Occasionally, the terminal ileum may be involved in ulcerative colitis due to "backwash ileitis," whereas it is the most common site of involvement in Crohn disease. The degree of wall thickening is significantly greater with Crohn disease than with ulcerative colitis. Wall thickening is usually eccentric on the mesenteric side, with pseudodiverticulum formation on the antimesenteric side (Fig 27). Frequently, there are skipped areas in Crohn disease, whereas ulcerative colitis is usually circumferential and continuous (Fig 28). Pseudopolyps (Fig 29) are a feature of ulcerative colitis when more extensive ulceration of the mucosa and submucosa develops and only scattered islands of normal mucosa remain. Pseudopolyps are characteristic of active disease. Abscess and fistula formation are common in Crohn disease but are not seen in ulcerative colitis. A halo of fat in the bowel wall is seen in chronic inflammatory bowel disease, more commonly in ulcerative colitis. On the other hand, the so-called comb sign is more commonly associated with active Crohn disease (4,21).
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Figure 26a. Crohn disease. (a) CT scan obtained with oral and intravenous contrast material shows wall thickening of the transverse colon with mural stratification (arrow). The engorged pericolonic vessels (arrowhead) are suggestive of active disease. Mild pericolonic fibrofatty proliferation is also present. (b) CT scan obtained with oral and intravenous contrast material shows marked wall thickening of the descending colon, cecum, and terminal ileum (arrowheads), findings that indicate diffuse colonic involvement.
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Figure 26b. Crohn disease. (a) CT scan obtained with oral and intravenous contrast material shows wall thickening of the transverse colon with mural stratification (arrow). The engorged pericolonic vessels (arrowhead) are suggestive of active disease. Mild pericolonic fibrofatty proliferation is also present. (b) CT scan obtained with oral and intravenous contrast material shows marked wall thickening of the descending colon, cecum, and terminal ileum (arrowheads), findings that indicate diffuse colonic involvement.
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Figure 27a. Pseudodiverticulum in a patient with Crohn disease. (a) CT scan obtained with oral and intravenous contrast material shows a pseudodiverticulum (arrow) at the antimesenteric side of a small bowel loop secondary to Crohn disease. Circumferential and eccentric mural thickening of the same loop is also present. (b) Image from a small bowel series helps confirm the presence of a pseudodiverticulum (arrow). A segmental ileal stricture and separation of loops due to fibrofatty proliferation are also noted.
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Figure 27b. Pseudodiverticulum in a patient with Crohn disease. (a) CT scan obtained with oral and intravenous contrast material shows a pseudodiverticulum (arrow) at the antimesenteric side of a small bowel loop secondary to Crohn disease. Circumferential and eccentric mural thickening of the same loop is also present. (b) Image from a small bowel series helps confirm the presence of a pseudodiverticulum (arrow). A segmental ileal stricture and separation of loops due to fibrofatty proliferation are also noted.
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Figure 28. Ulcerative colitis. CT scan obtained with oral contrast material shows diffuse circumferential concentric wall thickening of the colon (arrows). Mild associated fibrofatty proliferation of the mesentery is seen in the right side of the abdomen.
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Figure 29a. Pseudopolyps in a patient with proved ulcerative colitis. (a) CT scan obtained with oral and intravenous contrast material shows nodular circumferential concentric thickening of the descending colon with pseudopolyp formation (arrow). (b) Image from a barium enema examination helps confirm the presence of pseudopolyps (arrow) in the distal transverse and descending colon.
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Figure 29b. Pseudopolyps in a patient with proved ulcerative colitis. (a) CT scan obtained with oral and intravenous contrast material shows nodular circumferential concentric thickening of the descending colon with pseudopolyp formation (arrow). (b) Image from a barium enema examination helps confirm the presence of pseudopolyps (arrow) in the distal transverse and descending colon.
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Typhlitis.—
Typhlitis refers to the inflammation of the cecum often seen in immunosuppressed or neutropenic patients, usually after bone marrow transplantation. The cause is unknown but is probably multifactorial (ischemia, infection [especially cytomegalovirus], mucosal hemorrhage, and even neoplasm) (22). CT is the study of choice due to the commonly associated bowel dilatation and the increased risk of perforation. The cecum is usually distended, with circumferential wall thickening (Fig 30). Pericecal fat stranding tends to be severe. The patient’s medical history is crucial in suggesting the diagnosis.
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Figure 30. Typhlitis in a patient who was immunocompromised due to chemotherapy. CT scan obtained with oral and intravenous contrast material shows moderate circumferential wall thickening of the cecum (straight arrow) with surrounding fat stranding (curved arrow). Pneumatosis and contrast material are seen in the cecal wall (black arrowhead). The presence of a small amount of free air (white arrowhead) indicates perforation.
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Inflammatory Pseudotumor.—
Inflammatory pseudotumor consists of inflammatory and myo-fibroblastic spindle cells and may involve virtually any site in the body, most commonly the orbit and lung. Because inflammatory pseudotumor can mimic a malignancy both clinically and radiologically, the radiologist must be familiar with this rare entity to prevent unnecessary radical surgeries. In the gastrointestinal tract, ileocecal and gastric lesions are most frequently reported in young girls. At CT, pseudotumor manifests as a mass that is hypo- or isoattenuating relative to muscle. A mild degree of enhancement is usually present. Pseudotumor can produce bowel wall in-filtration, which manifests as focal circumferential wall thickening (apple core sign), and adjacent fat stranding (Fig 31). Mural calcifications have also been reported (23).
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Figure 31. Inflammatory pseudotumor. CT scan obtained with oral and intravenous contrast material shows marked concentric wall thickening of the rectum (arrow) with a narrowed lumen and severe surrounding fat stranding. Involvement of the sigmoid colon was also noted.
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Extraintestinal inflammatory processes may produce local or generalized bowel wall thickening due to contiguity. This phenomenon is exemplified by acute pancreatitis or intraperitoneal abscesses from any cause. In pancreatitis, the exudates of enzymes cause bowel irritation, most frequently in the duodenum, stomach, or transverse colon. Bowel dilatation secondary to ileus, fold thickening, and ascites are commonly present.
Autoimmune Causes
Autoimmune causes include collagen vascular disease and vasculitis, immunodeficiencies, and GVHD. Food allergies with gastrointestinal manifestations frequently diagnosed in children are included in this category.
Collagen Vascular Disease.—
Among the collagen vascular diseases, systemic lupus erythematosus and scleroderma are the most common causes of bowel disease, whereas periarteritis nodosa and Henoch-Schönlein purpura are the most common vasculitides. In collagen vascular diseases, deposition of circulating immune complexes produces necrotizing vasculitis of small arteries, arterioles, and venules throughout the body, which in turn leads to ischemia, hemorrhage, ulceration, and, occasionally, perforation. The small bowel is more commonly affected, usually in a concentric, segmental, or diffuse pattern (24). CT is very helpful in identifying other supportive signs of systemic involvement that are commonly associated with collagen vascular disease, such as polyserositis, renal involvement, or hepatosplenomegaly (Fig 32).
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Figure 32a. Systemic lupus erythematosus. (a) CT scan obtained with oral and intravenous contrast material shows thickened folds in the proximal jejunum (arrowhead). The peripheral cortical hypoattenuating area in the right kidney (arrow) represents a small infarct. (b) CT scan obtained with oral and intravenous contrast material shows diffuse wall thickening throughout the jejunum (arrow) secondary to active vasculitis.
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Figure 32b. Systemic lupus erythematosus. (a) CT scan obtained with oral and intravenous contrast material shows thickened folds in the proximal jejunum (arrowhead). The peripheral cortical hypoattenuating area in the right kidney (arrow) represents a small infarct. (b) CT scan obtained with oral and intravenous contrast material shows diffuse wall thickening throughout the jejunum (arrow) secondary to active vasculitis.
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Henoch-Schönlein purpura usually manifests with abdominal pain due to edema and intramural hemorrhage of the bowel preceding the skin rash. The radiologist may be the first to suggest the diagnosis. Gastrointestinal involvement occurs in more than 50% of affected patients. CT findings include multifocal bowel wall thickening with skipped areas (Fig 33), hyperattenuating bowel wall due to hemorrhage, bowel dilatation due to localized ileus, vascular engorgement (comb sign), and mesenteric edema. The presence of skipped areas may help differentiate Henoch-Schönlein purpura from other types of vasculitis (25). In a minority of patients, complications including intussusception, bowel ischemia, or perforation may be seen.
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Figure 33a. Henoch-Schönlein purpura. (a) CT scan obtained with oral and intravenous contrast material shows diffuse hyperattenuating concentric wall thickening of the jejunum (arrow) and ascites (arrowhead). No perforation was confirmed. (b) CT scan obtained with oral and intravenous contrast material shows diffuse hyperattenuating concentric wall thickening of a more distal jejunal loop (arrow), a finding that indicates the presence of skipped areas. Ascites is also seen (arrowhead).
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Figure 33b. Henoch-Schönlein purpura. (a) CT scan obtained with oral and intravenous contrast material shows diffuse hyperattenuating concentric wall thickening of the jejunum (arrow) and ascites (arrowhead). No perforation was confirmed. (b) CT scan obtained with oral and intravenous contrast material shows diffuse hyperattenuating concentric wall thickening of a more distal jejunal loop (arrow), a finding that indicates the presence of skipped areas. Ascites is also seen (arrowhead).
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Graft-versus-Host Disease.—
GVHD is a complication of allogenic bone marrow transplantation when the donor lymphocytes in the graft mount an immunologic attack against the host. The skin, gastrointestinal tract, and liver are the organs most commonly affected (26). A negative oral contrast agent should be the contrast material of choice in suspected cases of GVHD; such a contrast agent may make the commonly seen hyperattenuating mucosa more conspicuous. The CT findings may vary depending on the age of the process. Both the large and small bowel are involved, with the distal ileum most commonly affected. Varying degrees of concentric wall thickening with a hyperattenuating enhancing mucosa are seen (Fig 34). Prolonged coating of the bowel with oral contrast material is occasionally present, since the contrast material is incorporated into the submucosal layer through mucosal ulcers (Fig 35). This finding is highly suggestive of but not pathognomonic for GVHD, since it can also be seen with ischemia. Ascites and perienteric fat stranding can be seen in the acute setting. The presence of a stricture, a featureless segment of bowel, the so-called toothpaste appearance (also called moulage), or fibrofatty proliferation favors a chronic process (Fig 12).
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Figure 34. Acute GVHD. CT scan obtained with negative oral and intravenous contrast material shows diffuse small and large bowel wall thickening with a hyperattenuating mucosa (straight arrow) in the right lower quadrant. Associated dilated small bowel loops (curved arrow) and ascites (arrowhead) are seen in the left side of the pelvis.
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Figure 35. Acute GVHD. CT scan obtained with oral and intravenous contrast material shows a markedly hyperattenuating small bowel wall (arrow), a finding that is consistent with trapped contrast material dissecting under the mucosa. Massive ascites is also seen (arrowhead).
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Chronic Granulomatous Disease.—
Chronic granulomatous disease is an inherited disorder of neutrophil function characterized by recurrent infections by catalase-positive organisms. It affects the gastrointestinal tract from the esophagus to the rectum. Histologic analysis demonstrates inflammation with granuloma formation and in-filtration of lipid-laden histiocytes involving the lamina propria, smooth muscle, and serosa (27). No organisms are usually isolated from these lesions. Severe gastric antral and pyloric thickening is not the most common manifestation but a fairly typical one, leading to gastric outlet obstruction and acquired pyloric stenosis (Fig 36). Segmental thickening of the bowel wall, mesenteric lymph nodes with or without calcifications, hepatosplenomegaly, and abscesses are suggestive findings.
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Figure 36a. Chronic granulomatous disease in a 6-year-old patient. (a) CT scan obtained with oral and intravenous contrast material shows circumferential eccentric wall thickening of jejunal loops (arrowhead). Arrow indicates the inferior pole of an enlarged spleen. (b) Sagittal US image of the pylorus shows marked concentric wall thickening (arrows) with a narrowed lumen.
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Figure 36b. Chronic granulomatous disease in a 6-year-old patient. (a) CT scan obtained with oral and intravenous contrast material shows circumferential eccentric wall thickening of jejunal loops (arrowhead). Arrow indicates the inferior pole of an enlarged spleen. (b) Sagittal US image of the pylorus shows marked concentric wall thickening (arrows) with a narrowed lumen.
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Food Allergies with Gastrointestinal Manifestations.—
Food allergies are the result of a pathologic immune reaction to a food protein. In contrast, an adverse food reaction is an ill effect resulting from food ingestion and could be the result of an immunologic- or nonimmunologic-related response. Food intolerances of nonimmunologic cause may be secondary to an enzyme deficiency such as lactose intolerance or to a pharmacologic effect like those seen with preservatives and dyes. Such food intolerances are a rather common problem in children in whom the diagnosis is made clinically but could be identified at abdominal CT performed for the evaluation of chronic abdominal pain.
There are two types of immunoallergenic reactions producing gastrointestinal allergies: the IgE-mediated reaction and the T cell–mediated reaction. The eosinophilic gastroenteropathies are characterized by intense eosinophilic infiltration of the wall of the entire gastrointestinal tract. Gastric involvement is usually confined to the antrum, resulting in narrowing of the lumen (Fig 37). Patients usually complain of abdominal pain, anorexia, failure to thrive, protein-losing enteropathy, bleeding, and even ascites with associated peripheral eosinophilia. The disease is categorized as mucosal, intramural, or serosal, depending on the layer it involves. CT findings include concentric hypoattenuating thickening of the bowel wall due to mucosal fold thickening, which can be severe, causing peritoneal stranding, ascites, and even pleural effusions. If there is serosal involvement, the margins of the outer wall are indistinct. Celiac disease–gluten enteropathy is an example of a T cell–mediated chronic inflammatory process with an autoimmune component (28,29).
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Figure 37. Eosinophilic gastroenteritis. Coronal reconstructed image from CT data obtained with oral and intravenous contrast material shows severe, diffuse, concentric, hypoattenuating thickening of the small bowel wall (straight arrow). There is also severe wall thickening of the gastric rugae confined to the antrum (curved arrow) causing mild narrowing. The hypoattenuating appearance of the serosa (outer layer) of the gut causes indistinctness of the margins (arrowhead).
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Mechanical Causes
Mechanical causes of bowel wall thickening in pediatric patients include ischemia, intussusception, appendicitis, and, rarely, radiation enteritis.
Ischemia.—
Bowel ischemia does occur in children, although the cause is somewhat different than in adults. In adults, atherosclerosis, heart failure with low cardiac output, and use of vasopressor drugs account for the majority of cases. In children, midgut volvulus, congenital heart disease (Fig 38), and incarcerated hernias are common causes of bowel ischemia, with disastrous consequences to the patient if not diagnosed promptly. As mentioned earlier, certain diseases may be complicated by bowel ischemia, such as purpura and collagen vascular disease, hemolytic uremic syndrome, and typhlitis. Sickle cell disease can occasionally result in mesenteric ischemia as well. In premature newborns, necrotizing enterocolitis is a common cause affecting the distal ileum and colon and is usually evaluated with conventional radiography and US. Imaging features of bowel ischemia in children are the same as those in adults and include bowel dilatation, a nonenhancing bowel wall, circumferential wall thickening, and mural stratification (target sign). Pneumatosis is suggestive of advanced disease but not pathognomonic for ischemia, being associated with several causes described previously (6). CT is more sensitive than radiography in the diagnosis of pneumatosis.
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Figure 38a. Ischemia in a patient with congenital heart disease and Down syndrome. (a) CT scan obtained with oral and intravenous contrast material shows severe dilatation of the stomach with an air-fluid level and pneumatosis (arrow) extending to the duodenum. Marked concentric wall thickening of a fluid-filled duodenum (arrowhead) is seen producing mural stratification. (b) Coronal reconstructed image demonstrates a distended stomach with diffuse pneumatosis (arrow) and marked antral wall thickening (arrowhead).
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Figure 38b. Ischemia in a patient with congenital heart disease and Down syndrome. (a) CT scan obtained with oral and intravenous contrast material shows severe dilatation of the stomach with an air-fluid level and pneumatosis (arrow) extending to the duodenum. Marked concentric wall thickening of a fluid-filled duodenum (arrowhead) is seen producing mural stratification. (b) Coronal reconstructed image demonstrates a distended stomach with diffuse pneumatosis (arrow) and marked antral wall thickening (arrowhead).
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Intussusception.—
Although US is the test of choice in patients with suspected intussusception, this condition is occasionally encountered as an unexpected finding at CT (30). Intussusception is most commonly idiopathic, often manifesting after an upper respiratory infection. This type of intussusception is usually ileocolic. When intussusception is seen in the neonatal period or after 4 years of age, a lead point must be suspected. Common lead points include polyps (Fig 39), Meckel diverticulum, and lymphoma. Cystic fibrosis is also a cause in older children (31). Secondary intussusceptions may occur anywhere in the bowel. Focal bowel wall thickening with trapped mesenteric fat, sometimes simulating a mass, is seen at CT. There may be associated proximal bowel dilatation due to obstruction.
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Figure 39. Intussusception. CT scan obtained with oral and intravenous contrast material shows a small bowel intussusception in the left lower quadrant (arrow). Surgery revealed a polyp to be the lead point of the intussusception.
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Acute Appendicitis and Complications of Meckel Diverticulum.—
Acute appendicitis is an inflammatory condition caused by luminal obstruction of the appendix, usually at the base, leading to dilatation, inflammation, ischemia, and, ultimately, perforation. Imaging protocols for the evaluation of appendicitis in children are even more controversial than in adults. Radiation is a factor, and US is the first-line imaging modality at our institution, except in patients with a large body habitus or with inconclusive US findings. In thin patients, the lack of mesenteric fat makes the interpretation of a CT study more challenging. The use of negative oral contrast material may complicate interpretation, since the presence of intraluminal fluid is one of the suggestive findings. Other imaging findings of acute appendicitis include a dilated appendix thicker than 0.6 cm, circumferential wall thickening, wall enhancement after contrast material administration, and periappendiceal fat stranding (Fig 40). A radiopaque appendicolith is occasionally seen, making the diagnosis more certain (32). Without other signs of inflammation, however, the diagnosis of acute appendicitis cannot be made solely on the basis of the presence of an appendicolith. Intraluminal air is uncommon but can be seen in acute appendicitis. After perforation, the appendix may decompress and have a normal diameter, but free fluid, an abscess, and diffuse fat stranding are supporting findings.
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Figure 40. Appendicitis. CT scan obtained with oral and intravenous contrast material shows concentric wall thickening and enhancement (arrow) of a fluid-filled appendix with a distended lumen and surrounding fat stranding.
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Meckel diverticulum is a congenital anomaly caused by the incomplete obliteration of the vitelline duct. Most of the complications of this anomaly occur in children, the most common being gastrointestinal bleeding due to the presence of heterotopic gastric mucosa. Meckel diverticulitis is uncommon but can produce bowel wall thickening. CT demonstrates a blind-ending tubular structure arising from the antimesenteric border of the distal ileum, with associated wall thickening and fat stranding.
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Conclusions
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Although many bowel diseases affect both adults and children, some are unique to or more prevalent in pediatric patients. CT is an invaluable diagnostic tool in the evaluation of pediatric diseases involving the bowel, in spite of the use of ionizing radiation. Radiologists must be familiar with the CT signs of bowel disease and should take careful note of the bowel characteristics to generate an adequate differential diagnosis. The study should be tailored and optimized in advance according to the clinical scenario to decrease radiation exposure due to repeated or delayed scanning. With spiral CT scanners, studies can be performed quickly, thereby eliminating the need for sedation, and multiple reconstructed images may be generated.
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Footnotes
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Abbreviations: GVHD = graft-versus-host disease
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References
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Abstract
Introduction
