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DOI: 10.1148/radiol.2303020645
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(Radiology 2004;230:783-784.)
© RSNA, 2004


Signs in Imaging

The Comb Sign1

António J. Madureira, MD

1 From the Department of Radiology, Hospital S. João, University of Porto, R. S. João Bosco, 305–8 C, 4100–531 Porto, Portugal. Received May 31, 2002; revision requested July 18; revision received October 13; accepted December 19. Address correspondence to the author (e-mail: ajbmadureira@clix.pt).

Index terms: Crohn disease, 742.262 • Ileum • Intestines, CT, 742.1211 • Intestines, diseases, 742.262 • Signs in Imaging


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The comb sign is seen on contrast material–enhanced computed tomographic (CT) scans as multiple tubular, tortuous opacities on the mesenteric side of the ileum that are aligned as the teeth of a comb (Fig 1).



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Figure 1. Transverse CT scan of active Crohn disease with mesenteric hypervascularity in a 17-year-old female patient shows vascular dilatation, tortuosity, and enlargement of the vasa recta (small arrows) on the mesenteric side of the ileum—the comb sign. Affected ileal loops show mural thickening (arrowheads) (6 mm) and marked contrast enhancement of the mucosa. Also note fibrofatty proliferation of the mesentery, with diffuse increased attenuation of the mesenteric fat in this region as compared with that of the normal mesenteric fat (large arrow) on the opposite side.

 

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The arteries that supply the small bowel branch off within the mesentery as a series of intestinal arteries interconnected by arcades. The terminal branches, or vasa recta, are tall and widely spaced in the jejunum and are short and more closely arranged in the ileum (1). When contrast-enhanced CT depicts hypervascularity of the mesentery with vascular dilatation, tortuosity, and wide spacing of the vasa recta, the comb sign is produced. This is attributed to the increased flow and fibrofatty proliferation in the mesentery of the affected bowel (2).


    DISCUSSION
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Crohn disease is a chronic granulomatous process characterized by transmural inflammation of the bowel wall. It can involve any portion of the alimentary tract, but the terminal ileum and proximal colon are most commonly affected. The earliest macroscopic manifestations of this disease are enlarged lymphoid follicles and aphtoid ulcerations, which are demonstrable at double-contrast barium studies but are below the spatial resolution of CT (3).

The most common CT feature of Crohn disease is bowel wall thickening, which occurs in up to 82% of patients (4). Bowel wall thickening usually ranges between 5 and 10 mm but can reach 20 mm (Fig 2). This thickening is most frequently observed in the terminal ileum but can also affect other portions of the gastrointestinal tract. During the acute phase of the disease, the small bowel and colon maintain mural stratification, which results in a target or double-halo appearance at CT (3). This effect may be produced by submucosal edema or mural fat infiltration. Bowel wall thickening is not specific for Crohn disease and, in fact, it is primarily seen in up to 60% of patients with inactive ulcerative colitis and in only 8% of patients with Crohn disease (5). It may also be seen in radiation enteritis, graft versus host disease, and chronic ischemic bowel (6,7). Inflamed mucosa and serosa may show substantial contrast enhancement, and the intensity of enhancement relates to the clinical activity of the disease (3). In patients with long-standing disease and transmural fibrosis, mural stratification is lost, and the affected bowel wall typically has homogeneous attenuation on CT scans.



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Figure 2. Transverse CT scan in the same patient shows a long and tortuous segment of ileum with moderate mural thickening (7 mm) along bowel walls and luminal narrowing (arrowheads). There is some fluid in the lumen (arrows) and marked contrast enhancement of the mucosa, which are characteristic of Crohn disease.

 
The mesentery is frequently involved in Crohn disease. Fibrofatty proliferation of the mesentery, also known as creeping fat of the mesentery, is the most common cause of separation of bowel loops on small-bowel–series images in patients with Crohn disease (4). The sharp interface between bowel and mesentery is lost, and the attenuation value of fat is elevated by 20–60 HU because of the inflammatory changes that take place. Fibrofatty infiltration may resemble the comb sign only in part, in that the vessels will stand out on CT scans and will be separated from the serosal surface of the bowel and from each other. However, unlike with the comb sign, the vessels will not be abnormally thick and tortuous. Mesenteric lymph nodes may also be seen, and these usually range from 3 to 8 mm in size. If the lymph nodes are larger than 10 mm, the presence of lymphoma or carcinoma must be excluded, as both occur with greater frequency in patients with Crohn disease (8).

Hypervascularity of the mesentery with vascular dilatation, tortuosity, and prominence of the vasa recta, which together produce the comb sign, should suggest an acute exacerbation in patients with known Crohn disease. It has recently been reported that the presence of prominent perienteric vasculature seen at CT in patients with Crohn disease suggests that the disease is clinically active, advanced, and extensive (9). In patients presenting with clinical symptoms for the first time, these spiral CT findings should raise the possibility of this diagnosis but are not absolutely pathognomonic, as the comb sign has also been described in cases of lupus mesenteric vasculitis (10,11). In a study of patients with systemic lupus erythematosus who have acute abdominal pain, the comb sign was present in 87% of the cases in which there were CT findings of ischemic bowel disease (11).

There are several other disease processes in which engorgement of the mesenteric vessels has been reported, including vasculitis (such as polyarteritis nodosa, Henoch-Schönlein syndrome, microscopic polyangiitis, Behçet syndrome), mesenteric thromboembolism, strangulated bowel obstruction, and ulcerative colitis (3,1217). The clinical history, distribution of the disease, and associated findings are useful in the differential diagnosis of these diseases. The comb sign may be useful in the differential diagnosis of lymphoma and metastases, which are usually hypovascular lesions.

Complications of Crohn disease can be imaged with CT, which has been shown to affect patient treatment in 28% of cases (18). Abscesses (which occur in up to 20% of patients), fistulas, sinus tracts, and perianal disease are well depicted on CT scans. The systemic manifestations of the disease such as fatty infiltration of the liver, nephrolithiasis, cholelithiasis, sacroiliitis, and hydronephrosis should also be searched for when evaluating a CT scan of the abdomen in a patient with Crohn disease.


    FOOTNOTES
 
A trainee (resident or fellow) wishing to submit a manuscript for Signs in Imaging should first write to the Editor for approval of the sign to be prepared, to avoid duplicate preparation of the same sign.


    REFERENCES
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 EXPLANATION
 DISCUSSION
 REFERENCES
 

  1. Stallard DJ, Tu RK, Gould MJ, Pozniak MA, Pettersen JC. Minor vascular anatomy of the abdomen and pelvis: a CT atlas. RadioGraphics 1994; 14:493-513.[Abstract]
  2. Meyers MA, McGuire PV. Spiral CT demonstration of hypervascularity in Crohn disease: "vascular jejunization of the ileum" or the "comb sign.". Abdom Imaging 1995; 20:327-332.[CrossRef][Medline]
  3. Gore RM, Balthazar EJ, Ghahremani GG, Miller FH. CT features of ulcerative colitis and Crohn’s disease. AJR Am J Roentgenol 1996; 167:3-15.[Free Full Text]
  4. Goldberg HI, Gore RM, Margulis AR, Moss AA, Baker EL. Computed tomography in the evaluation of Crohn disease. AJR Am J Roentgenol 1983; 140:277-282.[Abstract/Free Full Text]
  5. Philpotts LE, Heiken JP, Westcott MA, Gore RM. Colitis: use of CT findings in differential diagnosis. Radiology 1994; 190:445-449.[Abstract/Free Full Text]
  6. Wills JS, Lobis IF, Denstman FJ. Crohn disease: state of the art. Radiology 1997; 202:597-610.[Free Full Text]
  7. Horton KM, Corl FM, Fishman EL. CT of nonneoplastic diseases of the small bowel: spectrum of disease. J Comput Assist Tomogr 1999; 23:417-428.[CrossRef][Medline]
  8. Gore RM. CT of inflammatory bowel disease. Radiol Clin North Am 1989; 27:717-730.[Medline]
  9. Lee SS, Ha HK, Yang SK, et al. CT of prominent pericolic or perienteric vasculature in patients with Crohn’s disease: correlation with clinical disease activity and findings on barium studies. AJR Am J Roentgenol 2002; 179:1029-1036.[Abstract/Free Full Text]
  10. Ko SF, Lee TY, Cheng TT, et al. CT findings at lupus mesenteric vasculitis. Acta Radiol 1997; 38:115-120.[Medline]
  11. Byun JY, Ha HK, Yu SY, et al. CT features of systemic lupus erythematosus in patients with acute abdominal pain: emphasis on ischemic bowel disease. Radiology 1999; 211:203-209.[Abstract/Free Full Text]
  12. Rha SE, Ha HK, Lee SH, et al. CT and MR imaging findings of bowel ischemia from various primary causes. RadioGraphics 2000; 20:29-42.[Abstract/Free Full Text]
  13. Jeong YK, Ha HK, Yoon CH, et al. Gastrointestinal involvement in Henoch-Schönlein syndrome: CT findings. AJR Am J Roentgenol 1997; 168:965-968.[Abstract/Free Full Text]
  14. Ha HK, Lee SH, Rha SE, et al. Radiologic features of vasculitis involving the gastrointestinal tract. RadioGraphics 2000; 20:779-794.[Abstract/Free Full Text]
  15. Ha HK, Lee HJ, Yang SK, et al. Intestinal Behçet syndrome: CT features of patients with and patients without complications. Radiology 1998; 209:449-454.[Abstract/Free Full Text]
  16. Kim JK, Ha HK, Byun JY, et al. CT differentiation of mesenteric ischemia due to vasculitis and thromboembolic disease. J Comput Assist Tomogr 2001; 25:604-611.[CrossRef][Medline]
  17. Balthazar EJ, Birnbaum BA, Megibow AJ, et al. Closed-loop and strangulating intestinal obstruction: CT signs. Radiology 1992; 185:769-775.[Abstract/Free Full Text]
  18. Fishman EK, Wolf EJ, Jones B, et al. CT evaluation in Crohn disease, effect on patient management. AJR Am J Roentgenol 1987; 148:537-549.[Abstract/Free Full Text]



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