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The diagnostic role of abdominal CT imaging findings in adults intussusception: Focused on the vascular compromise
European Journal of Radiology 62 (2007) 406–415
Review
The diagnostic role of abdominal CT imaging findings in adults intussusception: Focused on the vascular compromise Sung Bin Park, Hyun Kwon Ha ∗ , Ah Young Kim, Seung Soo Lee, Hye Jin Kim, Beom Jin Park, Yong Hyun Jin, Seong Ho Park, Kyoung Won Kim Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan, College of Medicine, # 388-1 Poongnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea Received 24 June 2006; received in revised form 29 December 2006; accepted 2 January 2007
Abstract Intussusception is defined as telescoping of one segment of the gastrointestinal tract into an adjacent one. Unlike that in children, adult intussusception is a relatively rare condition. More than 90% of patients with adult intussusception have been reported to have an organic cause, with benign or malignant tumors for accounting for approximately 65% of the cases. In general, the diagnosis is easily made by means of computed tomography (CT) or magnetic resonance (MR) imaging. The imaging appearance of a bowel-within-bowel configuration with or without contained fat and mesenteric vessels, is pathognomonic. As the intussusceptum enters into the intussuscipiens, the mesentery is carried forward and trapped between the overlapping layers of bowel. The twisting or severe constriction of the mesenteric vessels may result in vascular compromise with subsequent edematous thickening of the involved bowel. In these circumstances, ischemic necrosis may develop if timely intervention is not undertaken. Therefore, determination of the presence or absence of intestinal necrosis in intussusception is important in patient management. On CT, the presence of well-known diagnostic CT criteria for strangulated obstruction (especially severe engorgement or twisting of the mesenteric vessels) as well as evidence of loss of the layered pattern, accumulation of extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis. CT and MR imaging are limited in determining the primary disease causing intussusception. However, CT and MR provide excellent preoperative evaluation, including the possible extension and/or dissemination of a malignant tumor. CT and MR imaging may also be useful in suggesting the presence of vascular compromise. © 2007 Elsevier Ireland Ltd. All rights reserved. Keywords: Intussusception; Intestinal obstruction; Computed tomography; Magnetic resonance imaging
Contents 1. 2. 3. 4.
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Imaging findings of intussusception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Type and manifestation of intussusception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Imaging diagnosis of primary cause . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Signs of vascular compromise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Corresponding author. Tel.: +82 2 3010 4373x4400; fax: +82 2 476 4719. E-mail address: [email protected] (H.K. Ha).
0720-048X/$ – see front matter © 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2007.01.003
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S.B. Park et al. / European Journal of Radiology 62 (2007) 406–415
1. Introduction Intussusception is defined as telescoping of one segment of the gastrointestinal tract into an adjacent one. Unlike that in children, adult intussusception is a relatively rare condition. More than 90% of patients with adult intussusception have been reported to have an organic cause, with benign or malignant tumors for accounting for approximately 65% of the cases [1,2]. In general, the diagnosis is easily made by means of CT or MR imaging [3–6]. The imaging findings include a mass with sausage-like or target-like appearance, often containing fat and mesenteric vessels. However, imaging modalities are limited in determining the primary cause of intussusception as well as in determining the presence or absence of ischemic injury at the involved bowel segment, which requires immediate surgery. The purpose of this retrospective review is to show the usefulness of CT and MR imaging in 24 patients with adult intussusception in determining the primary cause of the intussusception as well as displaying the CT findings in cases with vascular compromise. 2. Materials and methods A computerized search was conducted for cases from January 1999 to December 2003 of intussusceptions. Of 355 patients identified, 62 had undergone CT for the evaluation of intussusception. However, 38 of these patients were excluded from the review because of the followings: CT scans were not available (n = 13), the causes of intussusception were not confirmed by surgery (n = 22), and the image quality of CT scans was very poor (n = 3). Our review population, therefore, consisted of 24 consecutively evaluated patients with enteroenteric type intussusception (n = 9), enterocolic type (n = 12), and colocolic type (n = 3). Among the enteroenteric type, presumed spontaneous reduction of intussusception (n = 1) is also included. The patients ranged in age from 19 to 80 years (mean, 48 years). There were
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10 women and 14 men. CT was available in 24 patients and MR imaging was also available in four of these patients. In most, CT scans were obtained using a single-detector helical CT scanner (Somatom Plus-S; Siemens, Erlangen, Germany) from the diaphragm to the symphysis pubis with a beam collimation of 5 or 7 mm, a pitch of 1.5 or 1.7, and image reconstruction increment of 5 mm. In most, contrast material (600–900 ml; E-Z-CAT [barium sulfate suspension concentrate], EZ-Em, Westbury, NY) was administrated orally 30–40 min before scanning. A second contrast material (100–120 ml of Lopamiro 300 [iopamidol], Bracco Diagnostics or Ultravist 300 [iopromide], Schering) was administrated at a rate 3.0 ml/s intravenous injection to all patients, with injection starting approximately 120 s before scanning. MR was performed using a 1.5T MR imager (Magnetom vision; Siemens Medical Systems, Erlangen, Germany). T1-weighted images (TR range/TE range 400–600/8–11) and T2-weighted images including HASTE sequence (TR range/TE range 3500–4500/100–120; echo train length 8; section thickness 4 mm; intersection gap 2 mm; field of view 15 cm; number of acquisition 3; matrix 512 × 512) were obtained. The water as negative contrast was administered. After a rapid bolus intravenous injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) T1-weighted images were obtained. The primary cause of intussusception was proven at the surgery in all patients and included 17 primary small and large intestine tumors (5 lymphomas, 3 adenocarcinomas, 3 lipomas, 2 harmatomatous polyps associated with Peutz-Jegher syndrome, 2 inflammatory fibroid polyps, 1 mucocele, and 1 leukemia), four secondary metastatic tumors from melanoma or lung cancer, two adhesive bands and adhesions, and one eosinophilic enterocolitis (Table 1). Six of the 24 patients demonstrated vascular compromise on surgery. On CT or MR imaging, the imaging findings of intussusception were evaluated by two radiologists (S.B.P., H.K.H.) in consensus and in a random order. Thereafter, we attempted to
Table 1 Types and causes of adult intussusception Underlying pathology
Primary tumor Lymphoma Colon cancer Hamartomatous polyp (Peutz-Jegher syndrome) Lipoma Inflammatory fibroid polyp Mucocele Leukemia
Types
Total (24)
Ileocolic
Colocolic
4 2 1
1
Ileoileal
Jejunojejunal
1 1 1
2
2 1 1
Total Secondary tumor Melanoma metastasis Lung cancer metastasis Eosinophilic ileocecal colitis
(17)
1 1
1 1
1
1
1
Total Post-op adhesion
5 3 2 3 2 1 1
3 1 1 (5) 2
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determine the primary cause of intussusception as well as to determine the presence or absence of vascular compromise in the bowel involved by intussusception. The CT criteria used in this review to determine the presence or absence of vascular compromise were as follows: configuration of obstructed bowel loop; bowel wall thickness (involved segment); contrast enhancement pattern of involved bowel wall; absence or presence of target or double-halo sign; nature of mesenteric changes and amount of ascites [7]. The mesentery on the CT images was specially evaluated for evidence of an unusual vascular course, thrombosis, vascular engorgement, and haziness. The mesenteric vascular course was considered unusual if the CT images showed a reversed position of the superior mesenteric artery and vein, a whirl sign or vessels converging to one area. Engorgement of mesenteric vessels was determined by comparing the appearance of the vessels in question with the mesentery vessels that were considered to be normal. Poor or no contrast enhancement of the bowel wall was identified when there was poor or no definition of the configuration of the bowel wall compared with that of the adjacent bowel wall. Prolonged bowel wall enhancement was identified if the bowel wall was of higher attenuation on CT images relative to normal bowel wall. The objective criteria used for certifying strangulation included surgical inspection and pathologic specimen results. During surgery, bowel viability was determined by the color and motility of the bowel and by the presence of arterial pulsation. If viability was questionable, a bowel segment was placed on a saline-moistened sponge for 15–20 min and was then
Fig. 1. Ileoileal intussusception due to lymphoma in a 19-year-old male. (A) Contrast-enhanced CT scan shows a mass (arrows) with target appearance in the ileal loop. Mesenteric vessels and fat tissues are seen in the center of the mass. (B) Contrast-enhanced CT scan shows a round soft tissue mass (small arrows) at the leading point.
re-examined. Strangulation was present when bowel showed discoloration or frank gangrene with loss of arterial pulsation. 3. Results CT and MR imaging were successful in making a correct diagnosis of intussusception. All cases of intussusception showed bowel-within-bowel configuration with or without contained fat and mesenteric vessels. In a case of three lipomas, the intussusception was identified on initial MR imaging as ileoileal intussusception but was not identified on follow up CT scan and presumed spontaneous reduction of intussusception. Depending on their orientation to the scanning axis, they may appear as either a round, target-shaped mass (n = 16) or as an oblong sausage-shaped mass (n = 8) (Figs. 1 and 2). The motion-insensitive, T2-weighted HASTE image demonstrated the intussusception most clearly as have a concentric ring
Fig. 2. Ileocolic intussusception due to colonic adenocarcinoma in a 68-yearold female. (A) Contrast-enhanced CT scan shows a cavitary colonic tumor (arrows) in the ascending colon along with invaginated mesenteric vessels into the intussuscipiens. (B and C) Contrast-enhanced CT scans show a cystic masslike structure (small arrows) at a leading point. At surgery, there was no evidence of a cystic mass proximal to the colonic carcinoma. Therefore, we presumed that the cystic mass-like structure may represent obstructed, fluid-filled cecum taking over the colonic tumor.
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Fig. 3. Colocolic intussusception due to appendiceal mucocele in a 63-yearold male. (A and B) Contrast-enhanced CT scans show heterogeneous bowel wall thickening due to mural edema as well as a cystic mass (arrows) at the leading point. (C) T2-weighted axial scan shows concentric ring appearance due to the high contrast resolution between the high signal intensity intraluminal fluid and the relatively low signal intensity bowel wall. On MR imaging, the intussusception could be clearly defined compared with its definition of the CT scan.
appearance due to the high contrast resolution between the high signal intensity intraluminal fluid and the relatively low signal intensity bowel wall (Fig. 3). The primary causes of intussusception were determined before surgery in only 29% (7/24). These causes included lipoma (n = 3), metastasis due to underlying malignancy (melanoma n = 3, lung cancer n = 1). The finding of a homogenous mass with Hounsfield units between −80 and −120 on CT and fat signal intensity on MR, are nearly pathognomonic for a lipoma (Fig. 4). Intussusception is assumed to represent a manifestation of metastasis (Figs. 5 and 6). The CT scan findings of 24 patients with strangulated or simple intussusceptions are shown in Table 2. Six of these 24 patients were proven to have vascular compromise and their imaging findings included diffuse mesenteric change or severe engorgement of the mesenteric vessels (n = 5) (Fig. 7), unusual mesenteric vascular course or twisting (whirl
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Fig. 4. Ileoileal intussusception due to lipoma in 25-year-old female. (A) Contrast-enhanced CT scan shows intussusception with a fat-containing mass (small arrow) at the site of the leading point. (B) Small bowel follow-through shows a round filling defect (black arrows) along with a coil spring appearance in the proximal bowel. (C) Photograph of the gross specimen shows a lipomatous mass (arrowheads) in the ileum.
sign) (n = 1) (Fig. 5), absence of or poor bowel wall contrast enhancement (n = 1) (Fig. 8), and heterogeneous bowel wall enhancement with a target appearance (n = 1) (Fig. 6). The CT findings of strangulated intussusception are shown in Table 3. One patient among those with strangulated intussusception showed no identifiable findings suggestive of strangulation, and two patients with simple intussusception showed severe engorgement of the mesenteric vessels (n = 1) or an unusual mesenteric vascular course or twisting (whirl sign) (n = 1) (Fig. 9). On the pathology report, intestinal ischemia and necrosis was confirmed six strangulated intussusceptions. 4. Discussion 4.1. Imaging findings of intussusception The diagnosis of intussusception is easily made by CT and MR imaging. The major CT features, as previously described,
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multilayered bowel walls are also accurately depicted on MR imaging (Fig. 3). The bowel wall of the intussuscipiens is thickened and demonstrates high signal intensity on T1-weighted and T2-weighted images: this reflects the appearance of extracellular methemoglobin due to mural hemorrhage and necrosis. On post-gadolinium, T1-weighted images minimal enhancement of the bowel wall was seen, presumably reflecting the diminished vascularity of ischemic bowel [5]. 4.2. Type and manifestation of intussusception
Fig. 5. Ileoileal intussusception caused by a metastatic small intestine neoplasm from lung cancer in a 59-year-old male. (A) Contrast-enhanced CT scan shows a soft tissue mass (arrows) in the ileum at the leading point. (B) Contrast-enhanced CT scan 2-cm cephalad to (A) shows twisting of the mesenteric vessels within the intussusceptum; the ‘twisting sign’ (small arrows) may indicate the presence of vascular compromise. On surgery, vascular compromise was confirmed. (C) Contrast-enhanced CT scan shows another metastatic mural nodule (arrowhead) in the dilated proximal intestinal loop.
[3] include: (1) an intraluminal soft-tissue mass with an eccentrically placed fatty area or attenuation representing the intussusceptum and the intussuscepted mesentery, respectively; (2) a reniform or bilobed mass with high attenuation peripherally and lower attenuation centrally. This appearance reflects the invaginated intussusceptum surrounded by thickened bowel wall; and (3) a sausage-shaped mass with alternating areas of low and high attenuation. The different areas of attenuation closely reflect the space between the wall, mesentery fat and/or intestinal fluid and gas (Figs. 1 and 2). CT cannot distinguish between the different layers of the bowel wall. These shortcomings may be overcome on MR imaging [8]. MR imaging provides nearly the same imaging features as those seen on CT. Because of the advantages of MR multiplanar capability, the mesenteric fat and vessels telescoping into the intussuscipiens can be well-demonstrated. Furthermore,
The intussusceptions can be divided into enteroenteric, ileocolic, and colocolic. In general, the majority of lead points in enteroenteric intussusceptions are benign, including benign neoplasm [9,10] (Fig. 4), Meckels’s diverticula [11–13], adhesions, lymphoid hyperplasia and adenitis, trauma, celiac disease [14], duplications [15], Hamartomatous polyp associated Peutz-Jeghers syndrome [16,17] (Fig. 10), HenochSchonleion purpura [18], and inflammatory lesions [19,20] (Fig. 11); small-bowel malignancy (either primary or metastatic) (Figs. 5 and 6) may account for 6–30% of all cases. Eight percent to 20% of cases may be idiopathic [21], and transient nonobstructing enteric cases associated with physiologic status have also been reported [3,22–28]. Intussusception was reported to occur in 21% of patients with colon polyposis and in 40% of patients with ileal polyposis [29]. The pathophysiologic mechanism for developing intussuseption in patients with polyps may include bowel irritation thereby stimulating peristaltic activity and abnormal contractions [1]. On the other hand, colocolic intussusception is more likely to have a malignant etiology. Post-operative intussusception in adults is also recognized as a distinct entity which may be related to a variety of predisposing factors such as suture lines, oversewn ileum in jejunoileal bypass, previous jejunostomy site, adhesions (Fig. 8), submucosal bowel edema, intestinal dysmotility, long intestinal tubes, and chronic bowel dilatation [1]. Intussusceptions in patients with AIDS are generally ileal-based and may Table 2 CT findings of 23 patients with strangulated or simple obstruction due to intussusception CT findings
Strangulated (n = 6)
Simple (n = 17)
1 2.25 ± 0.53 6.77 ± 2.17 1
0 2.34 ± 0.46 6.41 ± 2.12 0
5:1
5:12
Mesenteric change Vascular engorgement Unusual vascular course
5 1
1 1
Ascites (small amount)
2
4
Bowel wall change Target sign Wall thickness (mean ± S.D.) Involved segment length (mean ± S.D.) Poor or no contrast enhancement Types Small bowel:large bowel
Note: n are numbers of patients, except for bowel wall thickness and involved bowel segment length. A case of lipoma excluded on analysis because not identifiable on CT scan. S.D., standard deviation.
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Fig. 6. Ileoileal intussusception caused by metastatic melanoma to the ileum in a 55-year-old female. (A) Contrast-enhanced CT scan shows a polypoid mass (small arrows) with contained mesenteric fat. (B and C) Contrast-enhanced CT scans show a soft tissue mass (arrows) at the leading point. The bowel wall proximal to the obstructed site appears thickened and heterogeneously enhanced (small arrows) with a target appearance caused by mural edema. (D) Photograph of the gross specimen shows multiple metastatic tumors and bowel infarction.
be caused by lymphoma, atypical mycobacterial infection, or another unusual inflammatory process [30–32]. Presenting signs and symptoms of intussusception include recurrent intestinal obstruction, intermittent abdominal cramps, or rectal bleeding. Recent, spontaneous reduction of an intussusception may also present in symptomatic or asymptomatic patients and occurs more commonly than was previously reported. These intussusceptions are usually short-segment, small-bowel
Fig. 7. Ileocolic intussusception due to leukemic infiltration in the ileum in a 64year-old male who obtained only unenhanced CT due to his poor general physical condition. Unenhanced CT shows a sausage-like mass in the ascending colon (arrows). Note diffuse vascular engorgement in the mesentery (small arrows); vascular compromise was confirmed at surgery. On a pathologic specimen taken following right hemicolectomy, recent hemorrhage and focal necrosis were noted in the terminal ileum and ileocecal valve. On microscopic examination, the submucosa at the same site was heavily infiltrated with mononuclear cells. The findings suggest myelocytic leukemic infiltrates.
Fig. 8. Ileoileal intussusception due to postoperative adhesion of the ileum in a 55-year-old male. (A) Contrast-enhanced CT scan shows target-like intussusception with contained mesenteric fat (arrows). (B) Contrast-enhanced CT scan cephalad to (A) shows engorged mesenteric vessels (small arrows) and poor bowel wall contrast enhancement. Collapsed bowel loops (asterisks) are also noted. At surgery, vascular compromise was confirmed.
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Fig. 9. Ileocolic intussusception due to inflammatory fibroid polyp in the ileum of a 28-year-old female. (A and B) Contrast-enhanced CT scans show a heterogeneous and somewhat hypoattenuated mass (M), leading the intussusception. Note twisting of the mesenteric vessels (small arrows) along the intussusceptum as well as thickened bowel wall. At surgery, vascular compromise was not evident.
intussusceptions with no recognizable lead point. In asymptomatic patients, conservative observation is warranted [22,26]. 4.3. Imaging diagnosis of primary cause Although CT and MR imaging are sensitive for detecting intussusception, morphological analysis of the lead point may not provide the necessary clues in many instances in order to determine the primary cause, except in cases of lipoma (Fig. 4). In general, intussusceptions involving the colon in adults were more often related to a primary carcinoma of the colon (Fig. 2), and intussusception involving the small bowel was usually related to a benign tumor (Fig. 4) and less often to a malignant tumor, which was usually a metastatic lesion (Figs. 5 and 6). Approximately 65% are due to neoplasms with a somewhat higher rate in intussusceptions involving the colon than those involving only the small bowel. Malignant tumors are more common than benign tumors in the colon, with the reverse being true in the small bowel. According to the series by Warshauer and Lee [22], enteroenteric intussusceptions caused by non-neoplastic lesions were shorter in length, smaller in diameter, and less likely to be associated with obstruction; no neoplastic enteric intussusceptions were shorter than 3.6 cm or smaller than 3.4 cm in diameter. Recent, Lvoff et al. [26] suggested that intussusception length is the main factor in distinguishing the majority of self-limiting small-bowel intussusceptions detected on CT from the minority
Fig. 10. Ileocolic intussusception due to Peutz-Jeghers syndrome in a 28-yearold male. (A) Contrast-enhanced CT scan shows a polypoid soft tissue mass (arrows) at the leading point. (B) Double-contrast barium study of the colon shows a lobulated, irregularly shaped of mass (M) in the ascending colon. Also noted are multiple, small filling defects (small arrows) in the adjacent colonic mucosal surface, representing multiple harmatomatous polyps. (C) Photograph of the gross specimen shows a dark brownish, lobulated, polypoid mass (arrows) in the cecum and terminal ileum. Also noted are numerous whitish-pink, flat, and slightly elevated mucosal lesions (small arrows).
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Table 3 CT findings of strangulated intussusception in six patients Case no.
Age
Sex
Cause
Type
CT findings suggestive of strangulation
1 2 3 4 5 6
64 59 55 55 19 25
M M M M M M
Leukemia Lung Cancer metastasis Melanoma metastasis Postoperative Adhesion Lymphoma Lipoma
Ileocolic Ileoileal Ileoileal Ileoileal Ileoileal Ileoileal
Vascular engorgement Vascular engorgement unusual vascular course (twisting sign) Vascular engorgement heterogeneous enhancing target sign Vascular engorgement poor bowel wall enhancement Vascular engorgement
that require surgery, shorter than 3.5 cm is likely to be selflimiting. Spontaneous reduction of an intussusception may also present in symptomatic or symptomatic patients and occurs more commonly than previously reported. 4.4. Signs of vascular compromise Vascular compromise is relatively uncommon in adults with intussusception, but it may be severe and may require emergency surgery. As the intussusceptum enters into the intussuscipiens,
the mesentery is carried forward and trapped between the overlapping layers of bowel. The twisting or severe constriction of the mesenteric vessels may result in vascular compromise with subsequent edematous thickening of the involved bowel. Ischemic necrosis may develop if timely intervention is not undertaken in these circumstances. The determination of the presence or absence of intestinal necrosis in intussusception is important for optimal patient management. According to experimental and clinical studies by Merine et al. [3] and Iko et al. [4], CT findings of extensive bowel
Fig. 11. Diffuse mural edema following the reduction of the ileocolic intussusception caused by eosinophilic ileocecal enterocolitis in a 39-year-old male. (A) Contrast-enhanced CT scan shows a concentric type of mural edema (arrows) in the ascending colon. (B) Contrast-enhanced CT scan shows edematous bowel wall thickening (small arrows) of the terminal ileum. (C) Double-contrast barium study shows narrowing of the terminal ileum (small arrows) with a prominent and thickened ileocecal valve (arrows). (D) Photograph of the gross specimen following right hemicolectomy, shows a thickened ileocecal valve (small arrows) with granulomas and hypertrophic changes. On microscopic examination, the ileocecal valve was only prominently involved with diffuse eosinophilic infiltration into the mucosa and serosa; a few granulomas were also demonstrated in the submucosa of the valve.
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wall thickening with loss of fascial planes (in an experimental study) and reniform or bilobed shape with thickened walls (in a clinical study), suggest some degree of vascular insufficiency and warrants more urgent surgical intervention. However, the criteria for these CT patterns are unclear and their diagnostic accuracy has not been fully evaluated. Therefore, who were proven to have vascular compromise in our review, none showed these findings. In our review, 6 of the 24 patients who were proven to have vascular compromise showed imaging findings including diffuse mesenteric change or severe engorgement of the mesenteric vessels (n = 5), unusual mesenteric vascular course or twisting (whirl sign) (n = 1), absence of or poor bowel wall contrast enhancement (n = 1) and heterogeneous bowel wall enhancement with target appearance (n = 1). According to a series by Fujimoto et al. [33], the CT findings of a hypodense layer in the returning wall, fluid collection in the space surrounded by the returning wall, and gas collection in the space surrounded by the returning wall, can be useful in predicting the degree of vascular compromise in intussusception. In the latter two CT findings (fluid and gas collection in the space surrounded by the returning wall) were speculated vascular compromised intussusception such as ischemia and necrosis. When these findings are applied to our review, fluid collection in the space surrounded by the returning wall, was noted in only two of six cases of strangulated intussusception and was also shown in two cases of simple intussusception. In contrast to Fujimoto’s series, which analyzed primarily the intrinsic components of intussusception, our review analyzed the intrinsic components and extrinsic secondary changes. Therefore, On CT, the presence of severe mesentric vascular engorgement or twisting (whirl sign) of the mesenteric vessels as well as evidence of loss of the layered pattern, extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis [4,34]. The bowel necrosis may be confined to the intussuscepted segment or can extend to the longer segment of the bowel. In summary, on CT, the presence of well-known diagnostic CT criteria for strangulated obstruction, especially severe engorgement or twisting of the mesenteric vessels, as well as evidence of loss of the layered pattern, extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis as an urgent complication of intussusception. 5. Conclusion CT and MR imaging are limited in their ability to determine the primary cause of intussusception. However, CT and MR provide an excellent pre-operative evaluation, including the possible extension and/or dissemination of a malignant tumor. Also, they may be useful for suggesting the presence of vascular compromise. Acknowledgement The authors thank Bonnie Hami, MA, Haaga Radiology Research Office, Department of Radiology, University Hospi-
tals Health System, Cleveland, Ohio, for editorial assistance in preparing the manuscript. References [1] Agha FP. Intussusception in adults. AJR Am J Roentgenol 1986;146: 527–31. [2] Begos DG, Sandor A, Modlin IM. The diagnosis and management of adult intussusception. Am J Surg 1997;173:88–94. [3] Merine D, Fishman EK, Jones B, Siegelman SS. Enteroenteric intussusception: CT findings in nine patients. AJR Am J Roentgenol 1987;148:1129–32. [4] Iko BO, Teal JS, Siram SM, Chinwuba CE, Roux VJ, Scott VF. Computed tomography of adult colonic intussusception: clinical and experimental studies. AJR Am J Roentgenol 1984;143:769–72. [5] Marcos HB, Semelka RC, Worawattanakul S. Adult intussusception: demonstration by current MR techniques. Magn Reson Imaging 1997;15:1095–8. [6] Lorigan JG, DuBrow RA. The computed tomographic appearances and clinical significance of intussusception in adults with malignant neoplasms. Br J Radiol 1990;63:257–62. [7] Ha HK, Kim JS, Lee MS, et al. Differentiation of simple and strangulated small-bowel obstruction: usefulness of known CT criteria. Radiology 1997;204:507–12. [8] Blomqvist L, von Rosen A, Hindmarsh T. MR imaging of adult colo-rectal intussusception. A case report. Acta Radiol 1995;36:656–8. [9] Mansberg VJ, Mansberg G, Doust BD. Jejunojejunal intussusception secondary to leiomyoma. Australas Radiol 1996;40:72–4. [10] Lamki N, Woo CL, Watson Jr AB, Kim HS. Adenomyomatous hamartoma causing ileoileal intussusception in a young child. Clin Imaging 1993;17:183–5. [11] Kim G, Daneman A, Alton DJ, Myers M, Sandler A, Superina R. The appearance of inverted Meckel diverticulum with intussusception on air enema. Pediatr Radiol 1997;27:647–50. [12] Hamada T, Ishida O, Yasutomi M. Inverted Meckel diverticulum with intussusception: demonstration by CT. J Comput Assist Tomogr 1996;20:287–9. [13] Deutsch JP, Mariette D, Moukarbel N, Parc R, Tubiana JM. Gastroduodenal intussusception secondary to Menetrier’s disease. Abdom Imaging 1994;19:207–9. [14] Strobl PW, Warshauer DM. CT diagnosis of celiac disease. J Comput Assist Tomogr 1995;19:319–20. [15] Patenaude Y, Jequier S, Russo P. Duplication cysts of the distal ileum, acting as a lead point for intussusception. Radiographics 1993;13: 218–20. [16] Lynch PM. Polyposis syndrome. In: Haubrich WS, Schaffner F, Berk JE, editors. Gastroenterology. Philadelphia: WB Saunders; 1995. p. 1731–43. [17] Buch JL, Harned RK, Lichtenstein JE, Sobin LH. Peutz-Jegher syndrome. Radiographics 1992;12:365–78. [18] Glasier CM, Siegel MJ, McAlister WH, Shackelford GD. HenochSchonlein syndrome in children: gastrointestinal manifestations. AJR Am J Roentgenol 1981;136:1081–5. [19] Shah A, Roberts J, Lipsky H, Twersky Y, Hirth M, Chawla K. Enteroenteric intussusception: an unusual presentation of Crohn’s disease in an adult patient. Am J Gastroenterol 1995;90:2231–2. [20] Box JC, Tucker J, Watne AL, Lucas G. Eosinophilic colitis presenting as a left-sided colocolic intussusception with secondary large bowel obstruction: an uncommon entity with a rare presentation. Am Surg 1997;63:741–3. [21] Stubenbord WT, Thorbjarnarson B. Intussusception in adults. Ann Surg 1970;172:306–10. [22] Warshauer DM, Lee JK. Adult intussusception detected at CT or MR imaging: clinical-imaging correlation. Radiology 1999;212: 853–60. [23] Kornecki A, Daneman A, Navarro O, Connolly B, Manson D, Alton DJ. Spontaneous reduction of intussusception: clinical spectrum, management and outcome. Pediatr Radiol 2000;30:58–63.
S.B. Park et al. / European Journal of Radiology 62 (2007) 406–415 [24] Catalano O. Transient small bowel intussuscpetion: CT findings in adults. Br J Radiol 1997;70:805–8. [25] Swischuk LE, John SD, Swischuk PN. Spontaneous reduction of intussusception: verifications with US. Radiology 1994;192:269–71. [26] Lvoff N, Breiman RS, Coakley FV, Lu Y, Warren RS. Distinguishing features of self-limiting adult small-bowel intussusception identified at CT. Radiology 2003;227:68–72. [27] Strouse PJ, DiPietro MA, Saez F. Transient small-bowel intussusception in children on CT. Pediatr Radiol 2003;33:316–20. [28] Sandrasegaran K, Kopecky KK, Rajesh A, Lappas J. Proximal small bowel intussusceptions in adults: CT appearance and clinical significance. Abdom Imaging 2004;29:653–7. [29] Felix EL, Cohen MH, Bernstein AD, Schwartz JH. Adult intussusception: case report of recurrent intussusception and review of literature. Am J Surg 1976;131:758–61.
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[30] Cappell MS, Hassan T, Rosenthal S, Mascarenhas M. Gastrointestinal obstruction due to Mycobacterium avium intracellulare associated with the acquired immunodeficiency syndrome. Am J Gastroenterol 1992;87:1823–7. [31] Wood BJ, Kumar PN, Cooper C, Silverman PM, Zeman RK. AIDSassociated intussusception in young adults. J Clin Gastroenterol 1995;21:158–62. [32] Balthazar EJ, Reich CB, Pachter HL. The significance of small bowel intussusception in acquired immune deficiency syndrome. Am J Gastroenterol 1986;81:1073–5. [33] Fujimoto T, Fukuda T, Uetani M, et al. Unenhanced CT findings of vascular compromise in association with intussusceptions in adults. AJR Am J Roentgenol 2001;176:1167–71. [34] Bar-Ziv J, Solomon A. Computed tomography in adult intussusception. Gastrointest Radiol 1991;16:264–6.
Review
The diagnostic role of abdominal CT imaging findings in adults intussusception: Focused on the vascular compromise Sung Bin Park, Hyun Kwon Ha ∗ , Ah Young Kim, Seung Soo Lee, Hye Jin Kim, Beom Jin Park, Yong Hyun Jin, Seong Ho Park, Kyoung Won Kim Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan, College of Medicine, # 388-1 Poongnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea Received 24 June 2006; received in revised form 29 December 2006; accepted 2 January 2007
Abstract Intussusception is defined as telescoping of one segment of the gastrointestinal tract into an adjacent one. Unlike that in children, adult intussusception is a relatively rare condition. More than 90% of patients with adult intussusception have been reported to have an organic cause, with benign or malignant tumors for accounting for approximately 65% of the cases. In general, the diagnosis is easily made by means of computed tomography (CT) or magnetic resonance (MR) imaging. The imaging appearance of a bowel-within-bowel configuration with or without contained fat and mesenteric vessels, is pathognomonic. As the intussusceptum enters into the intussuscipiens, the mesentery is carried forward and trapped between the overlapping layers of bowel. The twisting or severe constriction of the mesenteric vessels may result in vascular compromise with subsequent edematous thickening of the involved bowel. In these circumstances, ischemic necrosis may develop if timely intervention is not undertaken. Therefore, determination of the presence or absence of intestinal necrosis in intussusception is important in patient management. On CT, the presence of well-known diagnostic CT criteria for strangulated obstruction (especially severe engorgement or twisting of the mesenteric vessels) as well as evidence of loss of the layered pattern, accumulation of extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis. CT and MR imaging are limited in determining the primary disease causing intussusception. However, CT and MR provide excellent preoperative evaluation, including the possible extension and/or dissemination of a malignant tumor. CT and MR imaging may also be useful in suggesting the presence of vascular compromise. © 2007 Elsevier Ireland Ltd. All rights reserved. Keywords: Intussusception; Intestinal obstruction; Computed tomography; Magnetic resonance imaging
Contents 1. 2. 3. 4.
5.
∗
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Imaging findings of intussusception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Type and manifestation of intussusception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Imaging diagnosis of primary cause . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Signs of vascular compromise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Corresponding author. Tel.: +82 2 3010 4373x4400; fax: +82 2 476 4719. E-mail address: [email protected] (H.K. Ha).
0720-048X/$ – see front matter © 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2007.01.003
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1. Introduction Intussusception is defined as telescoping of one segment of the gastrointestinal tract into an adjacent one. Unlike that in children, adult intussusception is a relatively rare condition. More than 90% of patients with adult intussusception have been reported to have an organic cause, with benign or malignant tumors for accounting for approximately 65% of the cases [1,2]. In general, the diagnosis is easily made by means of CT or MR imaging [3–6]. The imaging findings include a mass with sausage-like or target-like appearance, often containing fat and mesenteric vessels. However, imaging modalities are limited in determining the primary cause of intussusception as well as in determining the presence or absence of ischemic injury at the involved bowel segment, which requires immediate surgery. The purpose of this retrospective review is to show the usefulness of CT and MR imaging in 24 patients with adult intussusception in determining the primary cause of the intussusception as well as displaying the CT findings in cases with vascular compromise. 2. Materials and methods A computerized search was conducted for cases from January 1999 to December 2003 of intussusceptions. Of 355 patients identified, 62 had undergone CT for the evaluation of intussusception. However, 38 of these patients were excluded from the review because of the followings: CT scans were not available (n = 13), the causes of intussusception were not confirmed by surgery (n = 22), and the image quality of CT scans was very poor (n = 3). Our review population, therefore, consisted of 24 consecutively evaluated patients with enteroenteric type intussusception (n = 9), enterocolic type (n = 12), and colocolic type (n = 3). Among the enteroenteric type, presumed spontaneous reduction of intussusception (n = 1) is also included. The patients ranged in age from 19 to 80 years (mean, 48 years). There were
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10 women and 14 men. CT was available in 24 patients and MR imaging was also available in four of these patients. In most, CT scans were obtained using a single-detector helical CT scanner (Somatom Plus-S; Siemens, Erlangen, Germany) from the diaphragm to the symphysis pubis with a beam collimation of 5 or 7 mm, a pitch of 1.5 or 1.7, and image reconstruction increment of 5 mm. In most, contrast material (600–900 ml; E-Z-CAT [barium sulfate suspension concentrate], EZ-Em, Westbury, NY) was administrated orally 30–40 min before scanning. A second contrast material (100–120 ml of Lopamiro 300 [iopamidol], Bracco Diagnostics or Ultravist 300 [iopromide], Schering) was administrated at a rate 3.0 ml/s intravenous injection to all patients, with injection starting approximately 120 s before scanning. MR was performed using a 1.5T MR imager (Magnetom vision; Siemens Medical Systems, Erlangen, Germany). T1-weighted images (TR range/TE range 400–600/8–11) and T2-weighted images including HASTE sequence (TR range/TE range 3500–4500/100–120; echo train length 8; section thickness 4 mm; intersection gap 2 mm; field of view 15 cm; number of acquisition 3; matrix 512 × 512) were obtained. The water as negative contrast was administered. After a rapid bolus intravenous injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) T1-weighted images were obtained. The primary cause of intussusception was proven at the surgery in all patients and included 17 primary small and large intestine tumors (5 lymphomas, 3 adenocarcinomas, 3 lipomas, 2 harmatomatous polyps associated with Peutz-Jegher syndrome, 2 inflammatory fibroid polyps, 1 mucocele, and 1 leukemia), four secondary metastatic tumors from melanoma or lung cancer, two adhesive bands and adhesions, and one eosinophilic enterocolitis (Table 1). Six of the 24 patients demonstrated vascular compromise on surgery. On CT or MR imaging, the imaging findings of intussusception were evaluated by two radiologists (S.B.P., H.K.H.) in consensus and in a random order. Thereafter, we attempted to
Table 1 Types and causes of adult intussusception Underlying pathology
Primary tumor Lymphoma Colon cancer Hamartomatous polyp (Peutz-Jegher syndrome) Lipoma Inflammatory fibroid polyp Mucocele Leukemia
Types
Total (24)
Ileocolic
Colocolic
4 2 1
1
Ileoileal
Jejunojejunal
1 1 1
2
2 1 1
Total Secondary tumor Melanoma metastasis Lung cancer metastasis Eosinophilic ileocecal colitis
(17)
1 1
1 1
1
1
1
Total Post-op adhesion
5 3 2 3 2 1 1
3 1 1 (5) 2
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determine the primary cause of intussusception as well as to determine the presence or absence of vascular compromise in the bowel involved by intussusception. The CT criteria used in this review to determine the presence or absence of vascular compromise were as follows: configuration of obstructed bowel loop; bowel wall thickness (involved segment); contrast enhancement pattern of involved bowel wall; absence or presence of target or double-halo sign; nature of mesenteric changes and amount of ascites [7]. The mesentery on the CT images was specially evaluated for evidence of an unusual vascular course, thrombosis, vascular engorgement, and haziness. The mesenteric vascular course was considered unusual if the CT images showed a reversed position of the superior mesenteric artery and vein, a whirl sign or vessels converging to one area. Engorgement of mesenteric vessels was determined by comparing the appearance of the vessels in question with the mesentery vessels that were considered to be normal. Poor or no contrast enhancement of the bowel wall was identified when there was poor or no definition of the configuration of the bowel wall compared with that of the adjacent bowel wall. Prolonged bowel wall enhancement was identified if the bowel wall was of higher attenuation on CT images relative to normal bowel wall. The objective criteria used for certifying strangulation included surgical inspection and pathologic specimen results. During surgery, bowel viability was determined by the color and motility of the bowel and by the presence of arterial pulsation. If viability was questionable, a bowel segment was placed on a saline-moistened sponge for 15–20 min and was then
Fig. 1. Ileoileal intussusception due to lymphoma in a 19-year-old male. (A) Contrast-enhanced CT scan shows a mass (arrows) with target appearance in the ileal loop. Mesenteric vessels and fat tissues are seen in the center of the mass. (B) Contrast-enhanced CT scan shows a round soft tissue mass (small arrows) at the leading point.
re-examined. Strangulation was present when bowel showed discoloration or frank gangrene with loss of arterial pulsation. 3. Results CT and MR imaging were successful in making a correct diagnosis of intussusception. All cases of intussusception showed bowel-within-bowel configuration with or without contained fat and mesenteric vessels. In a case of three lipomas, the intussusception was identified on initial MR imaging as ileoileal intussusception but was not identified on follow up CT scan and presumed spontaneous reduction of intussusception. Depending on their orientation to the scanning axis, they may appear as either a round, target-shaped mass (n = 16) or as an oblong sausage-shaped mass (n = 8) (Figs. 1 and 2). The motion-insensitive, T2-weighted HASTE image demonstrated the intussusception most clearly as have a concentric ring
Fig. 2. Ileocolic intussusception due to colonic adenocarcinoma in a 68-yearold female. (A) Contrast-enhanced CT scan shows a cavitary colonic tumor (arrows) in the ascending colon along with invaginated mesenteric vessels into the intussuscipiens. (B and C) Contrast-enhanced CT scans show a cystic masslike structure (small arrows) at a leading point. At surgery, there was no evidence of a cystic mass proximal to the colonic carcinoma. Therefore, we presumed that the cystic mass-like structure may represent obstructed, fluid-filled cecum taking over the colonic tumor.
S.B. Park et al. / European Journal of Radiology 62 (2007) 406–415
Fig. 3. Colocolic intussusception due to appendiceal mucocele in a 63-yearold male. (A and B) Contrast-enhanced CT scans show heterogeneous bowel wall thickening due to mural edema as well as a cystic mass (arrows) at the leading point. (C) T2-weighted axial scan shows concentric ring appearance due to the high contrast resolution between the high signal intensity intraluminal fluid and the relatively low signal intensity bowel wall. On MR imaging, the intussusception could be clearly defined compared with its definition of the CT scan.
appearance due to the high contrast resolution between the high signal intensity intraluminal fluid and the relatively low signal intensity bowel wall (Fig. 3). The primary causes of intussusception were determined before surgery in only 29% (7/24). These causes included lipoma (n = 3), metastasis due to underlying malignancy (melanoma n = 3, lung cancer n = 1). The finding of a homogenous mass with Hounsfield units between −80 and −120 on CT and fat signal intensity on MR, are nearly pathognomonic for a lipoma (Fig. 4). Intussusception is assumed to represent a manifestation of metastasis (Figs. 5 and 6). The CT scan findings of 24 patients with strangulated or simple intussusceptions are shown in Table 2. Six of these 24 patients were proven to have vascular compromise and their imaging findings included diffuse mesenteric change or severe engorgement of the mesenteric vessels (n = 5) (Fig. 7), unusual mesenteric vascular course or twisting (whirl
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Fig. 4. Ileoileal intussusception due to lipoma in 25-year-old female. (A) Contrast-enhanced CT scan shows intussusception with a fat-containing mass (small arrow) at the site of the leading point. (B) Small bowel follow-through shows a round filling defect (black arrows) along with a coil spring appearance in the proximal bowel. (C) Photograph of the gross specimen shows a lipomatous mass (arrowheads) in the ileum.
sign) (n = 1) (Fig. 5), absence of or poor bowel wall contrast enhancement (n = 1) (Fig. 8), and heterogeneous bowel wall enhancement with a target appearance (n = 1) (Fig. 6). The CT findings of strangulated intussusception are shown in Table 3. One patient among those with strangulated intussusception showed no identifiable findings suggestive of strangulation, and two patients with simple intussusception showed severe engorgement of the mesenteric vessels (n = 1) or an unusual mesenteric vascular course or twisting (whirl sign) (n = 1) (Fig. 9). On the pathology report, intestinal ischemia and necrosis was confirmed six strangulated intussusceptions. 4. Discussion 4.1. Imaging findings of intussusception The diagnosis of intussusception is easily made by CT and MR imaging. The major CT features, as previously described,
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multilayered bowel walls are also accurately depicted on MR imaging (Fig. 3). The bowel wall of the intussuscipiens is thickened and demonstrates high signal intensity on T1-weighted and T2-weighted images: this reflects the appearance of extracellular methemoglobin due to mural hemorrhage and necrosis. On post-gadolinium, T1-weighted images minimal enhancement of the bowel wall was seen, presumably reflecting the diminished vascularity of ischemic bowel [5]. 4.2. Type and manifestation of intussusception
Fig. 5. Ileoileal intussusception caused by a metastatic small intestine neoplasm from lung cancer in a 59-year-old male. (A) Contrast-enhanced CT scan shows a soft tissue mass (arrows) in the ileum at the leading point. (B) Contrast-enhanced CT scan 2-cm cephalad to (A) shows twisting of the mesenteric vessels within the intussusceptum; the ‘twisting sign’ (small arrows) may indicate the presence of vascular compromise. On surgery, vascular compromise was confirmed. (C) Contrast-enhanced CT scan shows another metastatic mural nodule (arrowhead) in the dilated proximal intestinal loop.
[3] include: (1) an intraluminal soft-tissue mass with an eccentrically placed fatty area or attenuation representing the intussusceptum and the intussuscepted mesentery, respectively; (2) a reniform or bilobed mass with high attenuation peripherally and lower attenuation centrally. This appearance reflects the invaginated intussusceptum surrounded by thickened bowel wall; and (3) a sausage-shaped mass with alternating areas of low and high attenuation. The different areas of attenuation closely reflect the space between the wall, mesentery fat and/or intestinal fluid and gas (Figs. 1 and 2). CT cannot distinguish between the different layers of the bowel wall. These shortcomings may be overcome on MR imaging [8]. MR imaging provides nearly the same imaging features as those seen on CT. Because of the advantages of MR multiplanar capability, the mesenteric fat and vessels telescoping into the intussuscipiens can be well-demonstrated. Furthermore,
The intussusceptions can be divided into enteroenteric, ileocolic, and colocolic. In general, the majority of lead points in enteroenteric intussusceptions are benign, including benign neoplasm [9,10] (Fig. 4), Meckels’s diverticula [11–13], adhesions, lymphoid hyperplasia and adenitis, trauma, celiac disease [14], duplications [15], Hamartomatous polyp associated Peutz-Jeghers syndrome [16,17] (Fig. 10), HenochSchonleion purpura [18], and inflammatory lesions [19,20] (Fig. 11); small-bowel malignancy (either primary or metastatic) (Figs. 5 and 6) may account for 6–30% of all cases. Eight percent to 20% of cases may be idiopathic [21], and transient nonobstructing enteric cases associated with physiologic status have also been reported [3,22–28]. Intussusception was reported to occur in 21% of patients with colon polyposis and in 40% of patients with ileal polyposis [29]. The pathophysiologic mechanism for developing intussuseption in patients with polyps may include bowel irritation thereby stimulating peristaltic activity and abnormal contractions [1]. On the other hand, colocolic intussusception is more likely to have a malignant etiology. Post-operative intussusception in adults is also recognized as a distinct entity which may be related to a variety of predisposing factors such as suture lines, oversewn ileum in jejunoileal bypass, previous jejunostomy site, adhesions (Fig. 8), submucosal bowel edema, intestinal dysmotility, long intestinal tubes, and chronic bowel dilatation [1]. Intussusceptions in patients with AIDS are generally ileal-based and may Table 2 CT findings of 23 patients with strangulated or simple obstruction due to intussusception CT findings
Strangulated (n = 6)
Simple (n = 17)
1 2.25 ± 0.53 6.77 ± 2.17 1
0 2.34 ± 0.46 6.41 ± 2.12 0
5:1
5:12
Mesenteric change Vascular engorgement Unusual vascular course
5 1
1 1
Ascites (small amount)
2
4
Bowel wall change Target sign Wall thickness (mean ± S.D.) Involved segment length (mean ± S.D.) Poor or no contrast enhancement Types Small bowel:large bowel
Note: n are numbers of patients, except for bowel wall thickness and involved bowel segment length. A case of lipoma excluded on analysis because not identifiable on CT scan. S.D., standard deviation.
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Fig. 6. Ileoileal intussusception caused by metastatic melanoma to the ileum in a 55-year-old female. (A) Contrast-enhanced CT scan shows a polypoid mass (small arrows) with contained mesenteric fat. (B and C) Contrast-enhanced CT scans show a soft tissue mass (arrows) at the leading point. The bowel wall proximal to the obstructed site appears thickened and heterogeneously enhanced (small arrows) with a target appearance caused by mural edema. (D) Photograph of the gross specimen shows multiple metastatic tumors and bowel infarction.
be caused by lymphoma, atypical mycobacterial infection, or another unusual inflammatory process [30–32]. Presenting signs and symptoms of intussusception include recurrent intestinal obstruction, intermittent abdominal cramps, or rectal bleeding. Recent, spontaneous reduction of an intussusception may also present in symptomatic or asymptomatic patients and occurs more commonly than was previously reported. These intussusceptions are usually short-segment, small-bowel
Fig. 7. Ileocolic intussusception due to leukemic infiltration in the ileum in a 64year-old male who obtained only unenhanced CT due to his poor general physical condition. Unenhanced CT shows a sausage-like mass in the ascending colon (arrows). Note diffuse vascular engorgement in the mesentery (small arrows); vascular compromise was confirmed at surgery. On a pathologic specimen taken following right hemicolectomy, recent hemorrhage and focal necrosis were noted in the terminal ileum and ileocecal valve. On microscopic examination, the submucosa at the same site was heavily infiltrated with mononuclear cells. The findings suggest myelocytic leukemic infiltrates.
Fig. 8. Ileoileal intussusception due to postoperative adhesion of the ileum in a 55-year-old male. (A) Contrast-enhanced CT scan shows target-like intussusception with contained mesenteric fat (arrows). (B) Contrast-enhanced CT scan cephalad to (A) shows engorged mesenteric vessels (small arrows) and poor bowel wall contrast enhancement. Collapsed bowel loops (asterisks) are also noted. At surgery, vascular compromise was confirmed.
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Fig. 9. Ileocolic intussusception due to inflammatory fibroid polyp in the ileum of a 28-year-old female. (A and B) Contrast-enhanced CT scans show a heterogeneous and somewhat hypoattenuated mass (M), leading the intussusception. Note twisting of the mesenteric vessels (small arrows) along the intussusceptum as well as thickened bowel wall. At surgery, vascular compromise was not evident.
intussusceptions with no recognizable lead point. In asymptomatic patients, conservative observation is warranted [22,26]. 4.3. Imaging diagnosis of primary cause Although CT and MR imaging are sensitive for detecting intussusception, morphological analysis of the lead point may not provide the necessary clues in many instances in order to determine the primary cause, except in cases of lipoma (Fig. 4). In general, intussusceptions involving the colon in adults were more often related to a primary carcinoma of the colon (Fig. 2), and intussusception involving the small bowel was usually related to a benign tumor (Fig. 4) and less often to a malignant tumor, which was usually a metastatic lesion (Figs. 5 and 6). Approximately 65% are due to neoplasms with a somewhat higher rate in intussusceptions involving the colon than those involving only the small bowel. Malignant tumors are more common than benign tumors in the colon, with the reverse being true in the small bowel. According to the series by Warshauer and Lee [22], enteroenteric intussusceptions caused by non-neoplastic lesions were shorter in length, smaller in diameter, and less likely to be associated with obstruction; no neoplastic enteric intussusceptions were shorter than 3.6 cm or smaller than 3.4 cm in diameter. Recent, Lvoff et al. [26] suggested that intussusception length is the main factor in distinguishing the majority of self-limiting small-bowel intussusceptions detected on CT from the minority
Fig. 10. Ileocolic intussusception due to Peutz-Jeghers syndrome in a 28-yearold male. (A) Contrast-enhanced CT scan shows a polypoid soft tissue mass (arrows) at the leading point. (B) Double-contrast barium study of the colon shows a lobulated, irregularly shaped of mass (M) in the ascending colon. Also noted are multiple, small filling defects (small arrows) in the adjacent colonic mucosal surface, representing multiple harmatomatous polyps. (C) Photograph of the gross specimen shows a dark brownish, lobulated, polypoid mass (arrows) in the cecum and terminal ileum. Also noted are numerous whitish-pink, flat, and slightly elevated mucosal lesions (small arrows).
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Table 3 CT findings of strangulated intussusception in six patients Case no.
Age
Sex
Cause
Type
CT findings suggestive of strangulation
1 2 3 4 5 6
64 59 55 55 19 25
M M M M M M
Leukemia Lung Cancer metastasis Melanoma metastasis Postoperative Adhesion Lymphoma Lipoma
Ileocolic Ileoileal Ileoileal Ileoileal Ileoileal Ileoileal
Vascular engorgement Vascular engorgement unusual vascular course (twisting sign) Vascular engorgement heterogeneous enhancing target sign Vascular engorgement poor bowel wall enhancement Vascular engorgement
that require surgery, shorter than 3.5 cm is likely to be selflimiting. Spontaneous reduction of an intussusception may also present in symptomatic or symptomatic patients and occurs more commonly than previously reported. 4.4. Signs of vascular compromise Vascular compromise is relatively uncommon in adults with intussusception, but it may be severe and may require emergency surgery. As the intussusceptum enters into the intussuscipiens,
the mesentery is carried forward and trapped between the overlapping layers of bowel. The twisting or severe constriction of the mesenteric vessels may result in vascular compromise with subsequent edematous thickening of the involved bowel. Ischemic necrosis may develop if timely intervention is not undertaken in these circumstances. The determination of the presence or absence of intestinal necrosis in intussusception is important for optimal patient management. According to experimental and clinical studies by Merine et al. [3] and Iko et al. [4], CT findings of extensive bowel
Fig. 11. Diffuse mural edema following the reduction of the ileocolic intussusception caused by eosinophilic ileocecal enterocolitis in a 39-year-old male. (A) Contrast-enhanced CT scan shows a concentric type of mural edema (arrows) in the ascending colon. (B) Contrast-enhanced CT scan shows edematous bowel wall thickening (small arrows) of the terminal ileum. (C) Double-contrast barium study shows narrowing of the terminal ileum (small arrows) with a prominent and thickened ileocecal valve (arrows). (D) Photograph of the gross specimen following right hemicolectomy, shows a thickened ileocecal valve (small arrows) with granulomas and hypertrophic changes. On microscopic examination, the ileocecal valve was only prominently involved with diffuse eosinophilic infiltration into the mucosa and serosa; a few granulomas were also demonstrated in the submucosa of the valve.
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wall thickening with loss of fascial planes (in an experimental study) and reniform or bilobed shape with thickened walls (in a clinical study), suggest some degree of vascular insufficiency and warrants more urgent surgical intervention. However, the criteria for these CT patterns are unclear and their diagnostic accuracy has not been fully evaluated. Therefore, who were proven to have vascular compromise in our review, none showed these findings. In our review, 6 of the 24 patients who were proven to have vascular compromise showed imaging findings including diffuse mesenteric change or severe engorgement of the mesenteric vessels (n = 5), unusual mesenteric vascular course or twisting (whirl sign) (n = 1), absence of or poor bowel wall contrast enhancement (n = 1) and heterogeneous bowel wall enhancement with target appearance (n = 1). According to a series by Fujimoto et al. [33], the CT findings of a hypodense layer in the returning wall, fluid collection in the space surrounded by the returning wall, and gas collection in the space surrounded by the returning wall, can be useful in predicting the degree of vascular compromise in intussusception. In the latter two CT findings (fluid and gas collection in the space surrounded by the returning wall) were speculated vascular compromised intussusception such as ischemia and necrosis. When these findings are applied to our review, fluid collection in the space surrounded by the returning wall, was noted in only two of six cases of strangulated intussusception and was also shown in two cases of simple intussusception. In contrast to Fujimoto’s series, which analyzed primarily the intrinsic components of intussusception, our review analyzed the intrinsic components and extrinsic secondary changes. Therefore, On CT, the presence of severe mesentric vascular engorgement or twisting (whirl sign) of the mesenteric vessels as well as evidence of loss of the layered pattern, extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis [4,34]. The bowel necrosis may be confined to the intussuscepted segment or can extend to the longer segment of the bowel. In summary, on CT, the presence of well-known diagnostic CT criteria for strangulated obstruction, especially severe engorgement or twisting of the mesenteric vessels, as well as evidence of loss of the layered pattern, extraluminal fluid collection, and bowel perforation, may suggest the diagnosis of intestinal necrosis as an urgent complication of intussusception. 5. Conclusion CT and MR imaging are limited in their ability to determine the primary cause of intussusception. However, CT and MR provide an excellent pre-operative evaluation, including the possible extension and/or dissemination of a malignant tumor. Also, they may be useful for suggesting the presence of vascular compromise. Acknowledgement The authors thank Bonnie Hami, MA, Haaga Radiology Research Office, Department of Radiology, University Hospi-
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