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Radiologic evaluation and staging of small intestine neoplasms
European Journal of Radiology 42 (2002) 193– 205 www.elsevier.com/locate/ejrad
Radiologic evaluation and staging of small intestine neoplasms Mustafa Ugur Korman * Department of Radiology, Cerrahpasa Medical Faculty, Istanbul Uni6ersity, 34300 Kocamustafapasa, Istanbul, Turkey Received 24 January 2002; received in revised form 25 January 2002; accepted 28 January 2002
Abstract The small intestine is an uncommon location for neoplasms in either clinical or radiological practice. Because of its anatomic location and morphology, diagnosis of the diseases that affect small intestine pose difficulties. Symptoms are nonspecific and endoscopy is commonly unsatisfactory. Since early and definite diagnosis is crucial for prompt therapy, radiological imaging plays an essential role. Enteroclysis is the primary and effective radiologic modality in the evaluation of small bowel neoplasms. On the other hand, computed tomography should be the complementary radiologic method as well as for staging. In this review, the most common neoplasms of the small intestine and their common radiologic findings have been discussed. © 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Small intestine; Neoplasms; Enteroclysis; Computed tomography
1. Introduction Although small intestine (SI) comprises 75% of the total length and more than 90% of the mucosal surface of the gastrointestinal tract (GIT), it is a rare location for the development of neoplasms [1]. Less than 25% of benign and approximately 2% of malignant neoplasms of the entire GIT are SI neoplasms. The prevalence differ in autopsy and clinical series, that benign neoplasms constitute 74% of the autopsy series, while malignant neoplasms in symptomatic cases requiring surgery constitute 75% of the clinical series [2,3]. The reported age-adjusted incidence is 1 per 100000 population with a prevalence of 0.6% [4]. The rare occurrence of small intestinal malignancies can be explained by the fact that the small intestine is resistant to malignant degeneration. Besides this, the clinical and radiological methods are mostly insufficient in the diagnosis. The major clinical symptoms are lassitude, weight loss, abdominal pain and discomfort. Most of the cases are asymptomatic until the late stages of the disease. Also the relative rarity, and similarity of the
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manifestations to other conditions of the GIT decrease the suspicion of such a lesion when the patient presents with early symptoms [5,6]. Most malignant lesions of the small intestine have already metastasized at the time of diagnosis, which is certainly the factor most responsible for the poor prognosis of these lesions [7]. Probably the most significant problem in the delayed radiological diagnosis of SI neoplasms is the false negative radiographic examination. A false negative examination deflects the clinical work-up away from the SI, wasting time in eventually reaching a diagnosis [8]. The evolving technology of enterescopy can play a significant role in the diagnosis of SI tumors, but predominantly used instruments cover only limited length of small intestine and are no substitute for barium studies [9–11]. Radiologists, therefore, should assume a major role in the work-up of patients with possible SI neoplasms [12]. Benign and malignant tumors develop in all histologic components of the small intestine including epithelial cells, lymphoid tissues, lymphatics, vessels, nerves, and muscle [13,14]. More than 35 histologic types of SI neoplasms have been identified [15]. The cell-type of tumor is often characteristic for the portion of small intestine involved [12,13,15,16].
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2. Predisposing factors The development of small intestinal malignancies is associated with certain risk factors. Crohn’s disease is associated with a 100-fold increase for the development of SI tumors [17]. The SI tumor related to Crohn’s disease is generally multifocal, and especially seen in the by-passed segments of the ileum [18]. The SI tumors are usually observed at the 6th to 7th decade, and since Crohn’s disease is seen at younger age groups, the tumors are seen approximately 10 years earlier [19]. About 1% of patients with Crohn’s disease of the SI eventually develop a complicating adenocarcinoma [17]. Ileal adenocarcinoma secondary to ‘backwash’ ileitis has also been reported in patients with ulcerative colitis [20]. Celiac disease is associated with the development of SI lymphoma and to a lesser degree adenocarcinoma [21–24]. A number of cases of adenocarcinoma developing in ileostomies in patients with familial polyposis and ulcerative colitis have been reported [25]. Rare causes of adenocarcinoma have also been described in ileal pouches and ileal loop conduits [26– 28]. Patients with familial adenomatous polyposis, neurofibromatosis and Peutz– Jeghers syndromes are under risk for developing adenocarcinomas and should be carefully and periodically screened [29– 32]. Adenocarcinoma may also arise in elderly within a small intestinal duplication cyst and in Meckel’s diverticula [33]. Also Celiac disease and immunoproliferative SI disease, acquired immunodeficiency syndrome (AIDS) and nodular lymphoid hyperplasia may predispose to the develop-
ment of non-Hodgkin’s lymphoma in ileum [34]. Pelvic or abdominal irradiation also appears to increase the risk of developing both SI and colonic adenocarcinoma [35].
3. Clinical presentation SI tumors produce no specific symptoms. Nausea, vomiting, crampy abdominal pain, abdominal distention can be aggravated by eating, or hemorrhage. The most frequent symptom is abdominal pain [8,13,36]. Metastatic carcinoid tumors may present with flushing, while diarrhea may be seen in either the carcinoid or lymphoma cases [37–39]. Perforation is generally observed in cases with SI lymphomas and leiomyosarcomas [38]. Palpable abdominal masses are seen in sarcomas rather than adenocarcinomas. As a rule, symptoms are related to tumor size, location within the SI, blood supply, and tendency to undergo ulceration and necrosis.
4. Site of occurrence
4.1. Benign tumors Most common benign tumors of SI, such as adenoma, leiomyoma or lipoma are rarely found and are usually asymptomatic and diagnosed incidentally. They are commonly diagnosed as a invagination (Fig. 1).
Fig. 1. Polyp causing invagination. Axial CT section depicts ileoileal invagination secondary to a 3-cm polypoid mass (*). Small arrow represents the intussusseption and large arrow the mesenteric fat.
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common site of clinically significant carcinoid tumors [42]. They tend to congregate in the distal ileum, with nearly 40% located within 60 cm of the ileocecal valve with some spillage into the cecum. In approximately 5% of patients with lymphoma, the primary manifestation of disease occurs in the SI. Twenty percent of lymphomas in children present in this fashion, as lymphoma is the most common malignant SI tumor in childhood [43]. Lymphoma occurs most commonly in the ileum, particularly in the distal and terminal parts of the ileum [44]. Approximately 60% of smooth-muscle tumors of the SI are malignant. Leiomyosarcomas are the most common in the jejunum and ileum [45].
5. Morphology
5.1. Benign tumors Fig. 2. Hamartomatous polyp. Peutz –Jeghers syndrome patient with multiple hamartomatous polyps (arrows) in the jejunal loops, measuring less than 1 cm, on enteroclysis.
Adenomas are predominantly seen in the duodenum, especially the periampullary region. Leiomyoma is more common in jejunum than in ileum, while lipomas usually occur in the distal SI but occasionally are found more proximally [12]. The upper gut, particularly duodenum is affected in one-third of the patients with familial adenomatous polyposis. Peutz– Jeghers syndrome (PJS) consists of mucocutaneous pigmentation (circumoral, hands and feet) and gastrointestinal polyps (hamartomas) and has a Mendelian dominant inheritance (Fig. 2). The hamartomas of PJS can occur in anywhere in the GIT but are most frequent in the SI [31]. Lipoma is the most frequent triggering factor of intussusception seen in adults [40]. Hemangiomas occur predominantly in the jejunum but may occur throughout the GIT. Lymphangioma, fibroma and neurofibroma are other rarely seen benign neoplasms of the SI [12].
4.2. Malignant tumors Adenocarcinoma, carcinoid tumor, lymphoma and leiomyosarcoma are malignant tumors of the SI seen in order of frequency [12]. Direct extension to the SI by carcinomas of the stomach, pancreas, and large bowel, as well as separate metastatic deposits of adenocarcinoma, epidermoid carcinoma, transitional cell carcinoma and melanoma may also be seen [12]. The duodenum, especially the periampullary region is the most frequent location for SI adenocarcinoma [41]. Over 95% of all gastrointestinal carcinoids occur in the appendix, rectum and SI [34]. After the appendix the SI is the most common second location, and it is the most
They are usually 1–6 cm in size and are oval or spheric tumors. Typical adenomas are small (1–3 cm), smooth or lobulated polypoid lesions. Leiomyomas may be intramural, intraluminal, extraluminal and dumb-bell shaped. They are often umblicated with a central ulceration secondary to compromise of the vascular supply. Lipomas are characteristically solitary, relatively avascular and of variable size (1–6 cm) [12].
5.2. Malignant tumors Duodenal carcinomas are polypoid in 70%, ulcerated in 20% and infiltrative in 10%. In the jejunum and ileum, 75% of adenocarcinomas are annular, constricting, and particularly ulcerated; the remainders are polypoid and fungating [13,46]. SI carcinoids that come to surgery are usually small, 0.5–2 cm submucosal-intramural tumors that bulge slightly into the lumen. Occasionally, they become polypoid and cause intussusceptions or obstruction as they enlarge [36,47,48]. More often, carcinoid related obstructions are of lower grade and result from fibrosis rather than the mass effect of the tumor. Local seratonin output produces hypertrophy of the muscularis and fibrosis with crowding of folds, outline distortion and kinking of the lumen. This fibrosis is responsible for the fixation, kinking and angulation seen on the SI series and the stellate soft tissue density mass on CT scan examinations [13]. The incidence of metastases is related to tumor size, those less than 1.0 cm rarely metastasize [49]. Multiple carcinoid tumors occur in 30% of the cases, and they are associated with other gastrointestinal malignant tumors in 17–53% of the cases [49,50]. Grossly, intestinal lymphomas may be polypoid, ulcerative, constrictive or aneurismal, with the polypoid growth being most common. At times, multiple lymphomatous polyps can be found throughout the
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entire intestinal tract. In adults, the most common lymphoma is histiocytic, while in children it is the well-differentiated lymphocytic type [43,44,51]. Lymph nodes are involved in 50% of patients at the time of operation [44,51]. A poor prognosis is associated with large tumor size, ulceration, multicentric origin and presence of involved lymph nodes [44]. Leiomyosarcomas arise from the muscular coats of the bowel wall, and are most frequently subserosal and exoenteric. However, they may grow toward the bowel lumen and become polypoid. They assume a round or oval shape and frequently have a central area of mucosal ulceration that causes a high incidence of intestinal bleeding [45]. Metastatic lesions should be mentioned as malignant lesions of the SI. They may cause symptoms similar to primary intestinal neoplasms. Such metastatic lesions have been known to occur in cases of melanoma, carcinoma of cervix, and lung, breast and soft tissue tumors. Often these metastases to the SI cause obstruction and bleeding. Metastatic melanomas have a little stroma, and obstruction is rarely seen even in large tumors unless they cause intussusception [12]. In a patient with a known history of malignancy, obstructive symptoms or bleeding from the gastrointestinal tract, a metastatic lesion must be considered.
6. Imaging consideration The survival rate of SI malignancies has not been changed despite the diagnostic and operative technological advances during the last 4 decades. The prognosis is poor, since most malignant neoplasm unfortunately has metastasized at initial presentation [12]. Analysis of the contribution of the delay of diagnosis of SI tumors showed that the major delay occurred after medical help was sought by the patient. The delay before medical contact was only one-seventh of the delay after medical contact. Although radiologists were responsible for a minority of the physician’s errors, radiologic errors caused the longest periods of delay in diagnosis. This report concluded that only greater awareness of the SI as a potential source of unexplained abdominal symptoms would lead to more prompt use of sensitive methods of radiologic examination and thus to improvement of the patient’s prognosis [8]. Plain film radiography has limited use in the diagnosis. However, it demonstrates the air-fluid levels in the presence of obstruction and the calcified lesions. Except for the proximal jejunum, which can often be entered by colonoscope, the preoperative demonstration of a tumor of the mesenteric SI depends on contrast radiology, preferably a barium examination by the enteroclysis method. An abnormality shown by the SI follow-through (SIFT) examination, the most com-
mon used method in most institutions has been reported in 53– 83% of primary malignant tumors, although direct evidence of a tumor was noted in only 30–44% of cases [52–54]. In a study comparing the sensitivity and tumor detection rate of the enteroclysis and SIFT, the sensitivity was 61 and 95%, respectively. The actual tumor detection rate was 33% for the SIFT and 90% for enteroclysis [54]. Reported series have shown enteroclysis to be more reliable not only in the demonstration of small bowel tumors, but also in the evaluation of occult gastrointestinal bleeding and of intestinal obstruction [55–60]. Computed tomography (CT), ultrasonography, and magnetic resonance imaging are complementary to barium studies in detection of SI neoplasms. CT is playing an important role and certain patterns of CT findings allow a reasonable distinction to be made between benign and malignant SI tumors. In cases of certain benign tumors, such a lipoma and leiomyoma, may make it possible to suggest the specific diagnosis. A homogenous mass with Hounsefield units between −80 and − 120 is considered pathognomonic for lipoma. Extraluminal extension of malignant tumors, staging of lymphoma, and the identification of secondary mesenteric and hepatic disease is possible with CT. Because the most common presentation is with gastrointestinal bleeding, angiography and scintigraphy may be used for site of bleeding and localization of these tumors. Angiographic demonstration of tumor neovascularity without contrast agent extravasation may also be of diagnostic importance, especially in patients with chronic occult bleeding when other diagnostic studies, endoscopy and barium contrast have been negative [61]. Scintigraphy with technetium-labeled red blood cells may identify bleeding sites with blood loss rates as low as 0.1 ml/min [62]. SI tumors are difficult to diagnose due to the nonspecific nature of the symptoms and rare occurrence compared to other organ tumors. In addition, the anatomic location makes the diagnosis difficult. Their prognosis is worse, since they have already metastasized at the time of diagnosis. Therefore, earlier recognition is the major factor improving the prognosis. The imaging modality of choice in the diagnosis of SI tumors should be enteroclysis, followed by a contrast enhanced abdominal CT examination. These two imaging procedures are complementary to each other. Enteroclysis provides optimal wall distention and displays mucosal pattern well. CT demonstrates the extraluminal component of the tumor and aids in staging process.
6.1. Benign tumors Benign SI tumors display similar morphologic characteristics on barium studies, and are inadequate to differentiate the histologic types. Differential diagnosis
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Fig. 3. Leiomyoma. Abdominal CT section demonstrates an extramural growing smooth-contoured 3 cm mass (M) showing the same soft tissue density as the adjacent psoas muscle.
can thus be obtained in most instances by observing the location, the number of lesions, and radiographic features of the tumor [12]. Leiomyoma is the most common symptomatic benign SI tumor and occurs in the fifth decade of life. The most common clinical presentation is bleeding (67%) and obstruction (15%) [63]. Intramural, intraluminal and bidirectional (dumb-bell) tumors are seen as round or oval filling defects on barium examinations. Extraluminal lesions, however, may not be detected on barium examinations unless they are very large. Displacement of intestinal loops may be the only radiologic finding [12]. They produce sharply defined spheric or ovoid masses ranging from 1 to 10 cm in size, and display homogenous tissue density and uniform contrast enhancement on CT examination (Fig. 3). The malignant potential of leiomyomas is related mainly to the size and biologic behaviour of the tumor rather than their histologic appearances. Malignant muscle tumors are larger than benign tumors less uniform in shape and of variable attenuation’s on CT scans [64]. Adenomas are usually asymptomatic. They occur most commonly in the duodenum. SI adenomas are single, usually in older patients but occasionally multiple adenomas are present especially in those with variations of familial adenomatous polyposis or Gardner’s syndrome [65]. On barium studies, they appear as either sessile or pedunculated intraluminal defects (Fig. 4). The commonest clinical presentation of lipomas is with obstruction [40]. Barium contrast studies demonstrate a sharply demarcated, often pedunculated tumor that tends to conform the contour of the SI lumen. CT can establish the diagnosis of SI lipoma by showing its attenuation values to be consistent with fat (Fig. 5) [12].
In contrast to other benign SI tumors, which are often asymptomatic, 80% of hemangiomas produce significant symptoms [66]. Plain film of the abdomen occasionally will show calcified phleboliths in different locations in the abdomen, a result of normal positional changes of bowel loops. Barium studies rarely outline hemangiomatous polyps and are likely miss the usually shallow elevations, unless the presence of phleboliths draws attention to them [12]. Inflammatory fibroid polyps are usually solitary and they have been regarded as an exuberant host response to an unknown injury [67]. The SI is the second most common site for inflammatory fibroid polyp after gas-
Fig. 4. Adenomatous polyp. A solitary polyp (open arrow) 5 mm in size is seen in pelvic ileum on enteroclysis examination.
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Fig. 5. Lipoma. Abdominal CT section demonstrates a rounded intraluminal mass (arrow) of fatty density representing lipoma.
tric antrum. Patients are generally elderly and the lesions generally occur in the ileum (Fig. 6). They may be pedunculated and may reach a size in excess of 5 cm. Erosions and ulcerations of the polyps are frequent [12]. There are no distinctive features to differentiate it from other mural or intraluminal lesions of the GIT
[68]. Contrast studies may demonstrate a smooth rounded mass in the distal SI, like the other benign SI tumors [12]. Fibromas, lymphangiomas and other benign tumors can also occur in the SI. They cannot be differentiated radiographically from other benign tumors.
Fig. 6. Giant fibroid polyp. Enteroclysis in a case with a known history of Crohn’s disease demonstrates typical bird-beak appaerance of invagination (open arrows) as a result of a giant fibroid polyp (p) in distal ileum.
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6.2. Malignant tumors The usual location of the adenocarcinomas is within 25 cm of the duodenojejunal junction. A patient referred for an upper gastrointestinal series for abdominal pain, vomiting or occult gastrointestinal bleeding should have evaluation not only of the duodenum but also of the proximal loops of jejunum. A dilated proxi-
Fig. 9. Intestinal lymphoma. Diffuse concentric bowel wall thickening in a long segment of jejunum and associated multiple mesenteric lymphadenopathies are present on this abdominal CT examination.
Fig. 7. Adenocarcinoma. Classic ‘apple-core’ appearance (arrow) of adenocarcinoma of the proximal jejunum is displayed on enteroclysis, causing partial obstruction.
Fig. 10. Intestinal lymphoma (constructive form). Constructive narrowing, effacement of the folds and destruction of the mucosal pattern in a short intestinal segment (open arrow) is seen on enteroclysis examination.
Fig. 8. Carcinoid tumor. A constructive segment (open arrow) and resultant prestenotic dilatation due to the desmoplastic reaction of the carcinoid tumor is present on enteroclysis examination. The serosal component of the mass causes extrinsic impression (arrow) on the adjacent intestinal loops.
mal jejunum with retrained fluid observed in this extended upper gastrointestinal examination should alert the radiologist to a possible obstructive neoplasm and should be an indication to continue the procedure as a fluoroscopic SI study [12]. The usual radiologic abnormality of a primary adenocarcinoma of the mesenteric SI on barium examination is the ‘apple core’ lesion (Fig. 7) [69]. This is a short annular, circumferentially narrowed segment with features of mucosal destruction. It is frequently ulcer-
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ated and separated from normal bowel wall above and below it by overhanging edges. The malignant stricture is usually central in position, rigid, and without change of shape during compression [54,70]. Lymphomas or leiomyosarcomas may have a similar appearance, but they exhibit alterations of shape with compression, since they are softer [12]. It has been shown that most of the annular apple core type lesions of the SI are as a
result of metastasis commonly from a carcinoma of the colon [71]. Carcinoids only rarely present as annular lesions. The ulcerating form of adenocarcinoma appears as a short narrow lesion usually with an inconspicuous mostly central ulcer. Polypoid mass that intussuscepts is also a rare manifestation of adenocarcinoma. In their CT presentation adenocarcinomas are proximal solitary soft tissue masses causing lumen nar-
Fig. 11. Intestinal lymphoma (cavitary form). (a) Enteroclysis examination shows a large irregular pelvic cavity filled with contrast material. On both sides of the cavity entering and leaving ileal segments are seen. (b) CT section depicts the large cavity (C) which shows air-contrast levels sealed-off by ileal segments.
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Fig. 12. Intestinal lymphoma (aneurysmatic form). A very rare form of intestinal lymphoma which presents as a huge aneurysmatic dilatation of the jejunum on enteroclysis. The folds are not effaced.
rowing and obstruction [72,73]. The lesions may be heterogeneous in attenuation and show moderate enhancement after intravenous contrast medium administration. Mesenteric extension should be suggested in cases with large mesenteric masses with heterogeneous attenuation and associated asymmetric narrowing of SI wall. Regional lymph nodes, liver, peritoneal surfaces and ovaries may be involved by mesenteric spread [12]. The demonstration by enteroclysis or via a carefully performed fluoroscopic SIFT of a smoothly rounded mucosa elevation of about 5– 10 mm in diameter, located in the distal ileum should always plays a carcinoid tumor at the top of the differential diagnosis. In early carcinoids (B1 cm) that not yet involved mesenteric lymph nodes, resection can be curative [12]. Carcinoid tumor lacks radiodiagnostic features characteristic for it and it is indistinguishable from other lesions such as leiomyoma, lipoma, or adenoma. The presence of one or more additional polyps of similar appearance further supports diagnosis of carcinoid [74]. The mucosa overlying carcinoids can ulcerate and it may be possible to demonstrate a carcinoid ulcer by enteroclysis [12]. CT scans of a mesenteric metastasis in addition to the spoke-wheel arrangement due to the emanating fibrosis show it to contain calcifications in well over half of the cases. Fibrosis, as a result of seratonins desmoplastic reaction, is responsible for the fixation, kinking and angulation seen on the SI series (Fig. 8) and the stellate soft tissue density mass on CT scan examinations [12]. Primary SI lymphomas account for approximately
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5% of all lymphomas and represent about one third of all GIT lymphomas [12]. In contrast to adenocarcinoma and leiomyosarcoma, which tend to produce a focal or segmental lesion, lymphoma of the SI originate at multiple sites and extends along the axis of the SI (Fig. 9) [73]. Secondary GI lymphoma usually affects multiple sites: at autopsy, gross or microscopic evidence of GI involvement has been found in up to 50% of cases of disseminated lymphoma [74]. In both the primary and secondary forms, the stomach is the most commonly involved (51%) followed by the SI (33%) [12]. Most of the non-Hodgkin’s lymphomas are of B-cell type, except for the sprue-related T-cell lymphoma [75]. Hodgkin’s disease account for only about 1% of all malignant lymphomas of the GIT [76]. The principal radiologic presentation of SI lymphoma are; circumferential segmental infiltration (Fig. 10), endo-exoenteric disease with cavitation (Fig. 11), aneurysmal dilatation (Fig. 12), polypoid lesions, mesenteric nodal lymphoma with secondary infiltration of SI (Fig. 13), and the possible transformation of diffuse nodular lymphoid hyperplasia into lymphoma (Fig. 14). The infiltrating form generally displays moderate lumen widening and is the most common radiologic appearance, closely followed by the cavitary form [12]. Among all primary malignant tumors in the SI, leiomyosarcomas account for 9% of the cases. Benign leiomyoma and a leiomyosarcoma cannot be differentiated radiographically. Usually, smooth muscle cell tumors that are large or show significant ulceration are malignant [12]. Most of these tumors are slow growing and are associated with a long period of symptoms. Patients are often anemic due to recurrent melena arising from ulcerated component and may complain of abdominal discomfort or pain. Leiomyosarcomas usually appear as an extrinsic mass displacing SI loops, due to the predominant extraluminal growth pattern. Barium studies demonstrate a deformity of the SI segment from which the tumor originates. Flattening, streching and possible ulceration of the mucosa can be seen. Adjacent loops may adhere to the mass as a result of infiltration or tethering by the considerable saprophytic blood supply [12]. Because of the exoenteric growth type of leiomyosarcomas, the manifestations on barium studies tend to be more subtle than the CT findings. The more characteristic CT pattern of a leiomyosarcoma is that of a bulky lesion, growing exoenterically (Fig. 15) [77]. The soft tissue component of the tumor usually shows significant enhancement following intravenous contrast administration [12]. Liposarcoma, angiosarcoma, and fibrosarcoma of the SI are among those rare tumors of SI reported in the literature. They are indistinguishable from leiomyosarcomas [12].
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Fig. 13. Intestinal lymphoma (mesenteric nodal form). (a) Enteroclysis examination shows widely displaced loop of ileum with effacement in plica circulares; also note mild surrounding segment (arrow). (b) CT section demonstrates large mesenteric nodal mass surrounding the ileal segment.
6.3. Metastatic tumors Tumor cells can spread to the SI through intraperitoneal seeding, hematogeneous dissemination, and extension from an adjacent tumor mass either directly or through lymphatic channels [78,79]. The mechanism of tumor spread influences its radiographic appearance. Metastasis through intraperitoneal seeding is most commonly observed in the pelvic SI loops and ileocecal region. When metastases are deposited on the serosal
surface of a segment of the SI, rounded protrusions toward the lumen of lesions at least 1 cm in diameter can be demonstrated by a carefully performed contrast examination (Fig. 16). The folds may assume a curved appearance at the periphery of metastasis or may be seen stretched and ‘tacked down’. Metastatic infiltration and fixation of folds at the affected bowel edge are accentuated by a divergence of folds toward the unaffected side. Associated fibrous reaction may lead to angulation and tethering of folds [12]. The neoplastic implants, such as gastrointestinal, ovarian and uterine
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Fig. 14. Intestinal lymphoma (nodular form). Diffuse submucosal nodular pattern (open arrow) and a slight dilatation in the jejunum is seen on enteroclysis. The folds are not effaced.
in origin, typically grow in relation to the concave or mesenteric border of bowel loops and can incite fibrosis [79]. CT plays an important role in the radiologic demonstration of metastatic lesions in the mesentery, peritoneal surfaces, and lymph nodes as well as in the bowel wall [12].
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Fig. 16. Peritoneal metastasis. Partial obstruction of the intestinal loops (arrows) in several adjacent segments is seen on enteroclysis secondary to peritoneal metastases (primary over carcinoma).
Malignant lymphoma, bronchial carcinoma, especially large cell type, and breast carcinoma are the most common tumors that metastasize to SI hematogenously, in order of frequency. The early radiologic changes in hematogeneous metastases to SI are usually multiple nodules, seen mostly along the antimesenteric
Fig. 15. Leiomyosarcoma. An extramural growing lobulated-contoured pelvic mass originating from the intestinal wall is seen. The mass contains a punctate calcification (arrowhead) and an umblication (arrow) secondary to superficial ulceration.
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Fig. 17. Malignant melanoma metastasis. A large lobulated-contoured intraluminal mass (arrow) and bird-beak appearance (arrowhead) secondary to invagination is seen on enteroclysis.
border, where the vasa recta arborize into a rich submucosal plexus [12]. Metastases can be seen generally as polypoid masses. Infiltrating ulcerative lesions may be seen as well. The polypoid lesions are more common and tend to be large and multiple and have a worse prognosis [12]. Early melanoma metastases to SI usually exhibit a smooth rounded polypoid lesion of different sizes radiographically. The demonstration on barium examination of a nonobstructing, fairly large intraluminal mass favors the diagnosis of melanoma metastasis (Fig. 17) [12]. This is due to the softness of the highly cellular mass, which contains little stroma. Metastases from lung cancer to SI may be shown as single or multiple discrete intraluminal lesions, either flat or polypoid, which are frequently ulcerated [12].
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Radiologic evaluation and staging of small intestine neoplasms Mustafa Ugur Korman * Department of Radiology, Cerrahpasa Medical Faculty, Istanbul Uni6ersity, 34300 Kocamustafapasa, Istanbul, Turkey Received 24 January 2002; received in revised form 25 January 2002; accepted 28 January 2002
Abstract The small intestine is an uncommon location for neoplasms in either clinical or radiological practice. Because of its anatomic location and morphology, diagnosis of the diseases that affect small intestine pose difficulties. Symptoms are nonspecific and endoscopy is commonly unsatisfactory. Since early and definite diagnosis is crucial for prompt therapy, radiological imaging plays an essential role. Enteroclysis is the primary and effective radiologic modality in the evaluation of small bowel neoplasms. On the other hand, computed tomography should be the complementary radiologic method as well as for staging. In this review, the most common neoplasms of the small intestine and their common radiologic findings have been discussed. © 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Small intestine; Neoplasms; Enteroclysis; Computed tomography
1. Introduction Although small intestine (SI) comprises 75% of the total length and more than 90% of the mucosal surface of the gastrointestinal tract (GIT), it is a rare location for the development of neoplasms [1]. Less than 25% of benign and approximately 2% of malignant neoplasms of the entire GIT are SI neoplasms. The prevalence differ in autopsy and clinical series, that benign neoplasms constitute 74% of the autopsy series, while malignant neoplasms in symptomatic cases requiring surgery constitute 75% of the clinical series [2,3]. The reported age-adjusted incidence is 1 per 100000 population with a prevalence of 0.6% [4]. The rare occurrence of small intestinal malignancies can be explained by the fact that the small intestine is resistant to malignant degeneration. Besides this, the clinical and radiological methods are mostly insufficient in the diagnosis. The major clinical symptoms are lassitude, weight loss, abdominal pain and discomfort. Most of the cases are asymptomatic until the late stages of the disease. Also the relative rarity, and similarity of the
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manifestations to other conditions of the GIT decrease the suspicion of such a lesion when the patient presents with early symptoms [5,6]. Most malignant lesions of the small intestine have already metastasized at the time of diagnosis, which is certainly the factor most responsible for the poor prognosis of these lesions [7]. Probably the most significant problem in the delayed radiological diagnosis of SI neoplasms is the false negative radiographic examination. A false negative examination deflects the clinical work-up away from the SI, wasting time in eventually reaching a diagnosis [8]. The evolving technology of enterescopy can play a significant role in the diagnosis of SI tumors, but predominantly used instruments cover only limited length of small intestine and are no substitute for barium studies [9–11]. Radiologists, therefore, should assume a major role in the work-up of patients with possible SI neoplasms [12]. Benign and malignant tumors develop in all histologic components of the small intestine including epithelial cells, lymphoid tissues, lymphatics, vessels, nerves, and muscle [13,14]. More than 35 histologic types of SI neoplasms have been identified [15]. The cell-type of tumor is often characteristic for the portion of small intestine involved [12,13,15,16].
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2. Predisposing factors The development of small intestinal malignancies is associated with certain risk factors. Crohn’s disease is associated with a 100-fold increase for the development of SI tumors [17]. The SI tumor related to Crohn’s disease is generally multifocal, and especially seen in the by-passed segments of the ileum [18]. The SI tumors are usually observed at the 6th to 7th decade, and since Crohn’s disease is seen at younger age groups, the tumors are seen approximately 10 years earlier [19]. About 1% of patients with Crohn’s disease of the SI eventually develop a complicating adenocarcinoma [17]. Ileal adenocarcinoma secondary to ‘backwash’ ileitis has also been reported in patients with ulcerative colitis [20]. Celiac disease is associated with the development of SI lymphoma and to a lesser degree adenocarcinoma [21–24]. A number of cases of adenocarcinoma developing in ileostomies in patients with familial polyposis and ulcerative colitis have been reported [25]. Rare causes of adenocarcinoma have also been described in ileal pouches and ileal loop conduits [26– 28]. Patients with familial adenomatous polyposis, neurofibromatosis and Peutz– Jeghers syndromes are under risk for developing adenocarcinomas and should be carefully and periodically screened [29– 32]. Adenocarcinoma may also arise in elderly within a small intestinal duplication cyst and in Meckel’s diverticula [33]. Also Celiac disease and immunoproliferative SI disease, acquired immunodeficiency syndrome (AIDS) and nodular lymphoid hyperplasia may predispose to the develop-
ment of non-Hodgkin’s lymphoma in ileum [34]. Pelvic or abdominal irradiation also appears to increase the risk of developing both SI and colonic adenocarcinoma [35].
3. Clinical presentation SI tumors produce no specific symptoms. Nausea, vomiting, crampy abdominal pain, abdominal distention can be aggravated by eating, or hemorrhage. The most frequent symptom is abdominal pain [8,13,36]. Metastatic carcinoid tumors may present with flushing, while diarrhea may be seen in either the carcinoid or lymphoma cases [37–39]. Perforation is generally observed in cases with SI lymphomas and leiomyosarcomas [38]. Palpable abdominal masses are seen in sarcomas rather than adenocarcinomas. As a rule, symptoms are related to tumor size, location within the SI, blood supply, and tendency to undergo ulceration and necrosis.
4. Site of occurrence
4.1. Benign tumors Most common benign tumors of SI, such as adenoma, leiomyoma or lipoma are rarely found and are usually asymptomatic and diagnosed incidentally. They are commonly diagnosed as a invagination (Fig. 1).
Fig. 1. Polyp causing invagination. Axial CT section depicts ileoileal invagination secondary to a 3-cm polypoid mass (*). Small arrow represents the intussusseption and large arrow the mesenteric fat.
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common site of clinically significant carcinoid tumors [42]. They tend to congregate in the distal ileum, with nearly 40% located within 60 cm of the ileocecal valve with some spillage into the cecum. In approximately 5% of patients with lymphoma, the primary manifestation of disease occurs in the SI. Twenty percent of lymphomas in children present in this fashion, as lymphoma is the most common malignant SI tumor in childhood [43]. Lymphoma occurs most commonly in the ileum, particularly in the distal and terminal parts of the ileum [44]. Approximately 60% of smooth-muscle tumors of the SI are malignant. Leiomyosarcomas are the most common in the jejunum and ileum [45].
5. Morphology
5.1. Benign tumors Fig. 2. Hamartomatous polyp. Peutz –Jeghers syndrome patient with multiple hamartomatous polyps (arrows) in the jejunal loops, measuring less than 1 cm, on enteroclysis.
Adenomas are predominantly seen in the duodenum, especially the periampullary region. Leiomyoma is more common in jejunum than in ileum, while lipomas usually occur in the distal SI but occasionally are found more proximally [12]. The upper gut, particularly duodenum is affected in one-third of the patients with familial adenomatous polyposis. Peutz– Jeghers syndrome (PJS) consists of mucocutaneous pigmentation (circumoral, hands and feet) and gastrointestinal polyps (hamartomas) and has a Mendelian dominant inheritance (Fig. 2). The hamartomas of PJS can occur in anywhere in the GIT but are most frequent in the SI [31]. Lipoma is the most frequent triggering factor of intussusception seen in adults [40]. Hemangiomas occur predominantly in the jejunum but may occur throughout the GIT. Lymphangioma, fibroma and neurofibroma are other rarely seen benign neoplasms of the SI [12].
4.2. Malignant tumors Adenocarcinoma, carcinoid tumor, lymphoma and leiomyosarcoma are malignant tumors of the SI seen in order of frequency [12]. Direct extension to the SI by carcinomas of the stomach, pancreas, and large bowel, as well as separate metastatic deposits of adenocarcinoma, epidermoid carcinoma, transitional cell carcinoma and melanoma may also be seen [12]. The duodenum, especially the periampullary region is the most frequent location for SI adenocarcinoma [41]. Over 95% of all gastrointestinal carcinoids occur in the appendix, rectum and SI [34]. After the appendix the SI is the most common second location, and it is the most
They are usually 1–6 cm in size and are oval or spheric tumors. Typical adenomas are small (1–3 cm), smooth or lobulated polypoid lesions. Leiomyomas may be intramural, intraluminal, extraluminal and dumb-bell shaped. They are often umblicated with a central ulceration secondary to compromise of the vascular supply. Lipomas are characteristically solitary, relatively avascular and of variable size (1–6 cm) [12].
5.2. Malignant tumors Duodenal carcinomas are polypoid in 70%, ulcerated in 20% and infiltrative in 10%. In the jejunum and ileum, 75% of adenocarcinomas are annular, constricting, and particularly ulcerated; the remainders are polypoid and fungating [13,46]. SI carcinoids that come to surgery are usually small, 0.5–2 cm submucosal-intramural tumors that bulge slightly into the lumen. Occasionally, they become polypoid and cause intussusceptions or obstruction as they enlarge [36,47,48]. More often, carcinoid related obstructions are of lower grade and result from fibrosis rather than the mass effect of the tumor. Local seratonin output produces hypertrophy of the muscularis and fibrosis with crowding of folds, outline distortion and kinking of the lumen. This fibrosis is responsible for the fixation, kinking and angulation seen on the SI series and the stellate soft tissue density mass on CT scan examinations [13]. The incidence of metastases is related to tumor size, those less than 1.0 cm rarely metastasize [49]. Multiple carcinoid tumors occur in 30% of the cases, and they are associated with other gastrointestinal malignant tumors in 17–53% of the cases [49,50]. Grossly, intestinal lymphomas may be polypoid, ulcerative, constrictive or aneurismal, with the polypoid growth being most common. At times, multiple lymphomatous polyps can be found throughout the
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entire intestinal tract. In adults, the most common lymphoma is histiocytic, while in children it is the well-differentiated lymphocytic type [43,44,51]. Lymph nodes are involved in 50% of patients at the time of operation [44,51]. A poor prognosis is associated with large tumor size, ulceration, multicentric origin and presence of involved lymph nodes [44]. Leiomyosarcomas arise from the muscular coats of the bowel wall, and are most frequently subserosal and exoenteric. However, they may grow toward the bowel lumen and become polypoid. They assume a round or oval shape and frequently have a central area of mucosal ulceration that causes a high incidence of intestinal bleeding [45]. Metastatic lesions should be mentioned as malignant lesions of the SI. They may cause symptoms similar to primary intestinal neoplasms. Such metastatic lesions have been known to occur in cases of melanoma, carcinoma of cervix, and lung, breast and soft tissue tumors. Often these metastases to the SI cause obstruction and bleeding. Metastatic melanomas have a little stroma, and obstruction is rarely seen even in large tumors unless they cause intussusception [12]. In a patient with a known history of malignancy, obstructive symptoms or bleeding from the gastrointestinal tract, a metastatic lesion must be considered.
6. Imaging consideration The survival rate of SI malignancies has not been changed despite the diagnostic and operative technological advances during the last 4 decades. The prognosis is poor, since most malignant neoplasm unfortunately has metastasized at initial presentation [12]. Analysis of the contribution of the delay of diagnosis of SI tumors showed that the major delay occurred after medical help was sought by the patient. The delay before medical contact was only one-seventh of the delay after medical contact. Although radiologists were responsible for a minority of the physician’s errors, radiologic errors caused the longest periods of delay in diagnosis. This report concluded that only greater awareness of the SI as a potential source of unexplained abdominal symptoms would lead to more prompt use of sensitive methods of radiologic examination and thus to improvement of the patient’s prognosis [8]. Plain film radiography has limited use in the diagnosis. However, it demonstrates the air-fluid levels in the presence of obstruction and the calcified lesions. Except for the proximal jejunum, which can often be entered by colonoscope, the preoperative demonstration of a tumor of the mesenteric SI depends on contrast radiology, preferably a barium examination by the enteroclysis method. An abnormality shown by the SI follow-through (SIFT) examination, the most com-
mon used method in most institutions has been reported in 53– 83% of primary malignant tumors, although direct evidence of a tumor was noted in only 30–44% of cases [52–54]. In a study comparing the sensitivity and tumor detection rate of the enteroclysis and SIFT, the sensitivity was 61 and 95%, respectively. The actual tumor detection rate was 33% for the SIFT and 90% for enteroclysis [54]. Reported series have shown enteroclysis to be more reliable not only in the demonstration of small bowel tumors, but also in the evaluation of occult gastrointestinal bleeding and of intestinal obstruction [55–60]. Computed tomography (CT), ultrasonography, and magnetic resonance imaging are complementary to barium studies in detection of SI neoplasms. CT is playing an important role and certain patterns of CT findings allow a reasonable distinction to be made between benign and malignant SI tumors. In cases of certain benign tumors, such a lipoma and leiomyoma, may make it possible to suggest the specific diagnosis. A homogenous mass with Hounsefield units between −80 and − 120 is considered pathognomonic for lipoma. Extraluminal extension of malignant tumors, staging of lymphoma, and the identification of secondary mesenteric and hepatic disease is possible with CT. Because the most common presentation is with gastrointestinal bleeding, angiography and scintigraphy may be used for site of bleeding and localization of these tumors. Angiographic demonstration of tumor neovascularity without contrast agent extravasation may also be of diagnostic importance, especially in patients with chronic occult bleeding when other diagnostic studies, endoscopy and barium contrast have been negative [61]. Scintigraphy with technetium-labeled red blood cells may identify bleeding sites with blood loss rates as low as 0.1 ml/min [62]. SI tumors are difficult to diagnose due to the nonspecific nature of the symptoms and rare occurrence compared to other organ tumors. In addition, the anatomic location makes the diagnosis difficult. Their prognosis is worse, since they have already metastasized at the time of diagnosis. Therefore, earlier recognition is the major factor improving the prognosis. The imaging modality of choice in the diagnosis of SI tumors should be enteroclysis, followed by a contrast enhanced abdominal CT examination. These two imaging procedures are complementary to each other. Enteroclysis provides optimal wall distention and displays mucosal pattern well. CT demonstrates the extraluminal component of the tumor and aids in staging process.
6.1. Benign tumors Benign SI tumors display similar morphologic characteristics on barium studies, and are inadequate to differentiate the histologic types. Differential diagnosis
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Fig. 3. Leiomyoma. Abdominal CT section demonstrates an extramural growing smooth-contoured 3 cm mass (M) showing the same soft tissue density as the adjacent psoas muscle.
can thus be obtained in most instances by observing the location, the number of lesions, and radiographic features of the tumor [12]. Leiomyoma is the most common symptomatic benign SI tumor and occurs in the fifth decade of life. The most common clinical presentation is bleeding (67%) and obstruction (15%) [63]. Intramural, intraluminal and bidirectional (dumb-bell) tumors are seen as round or oval filling defects on barium examinations. Extraluminal lesions, however, may not be detected on barium examinations unless they are very large. Displacement of intestinal loops may be the only radiologic finding [12]. They produce sharply defined spheric or ovoid masses ranging from 1 to 10 cm in size, and display homogenous tissue density and uniform contrast enhancement on CT examination (Fig. 3). The malignant potential of leiomyomas is related mainly to the size and biologic behaviour of the tumor rather than their histologic appearances. Malignant muscle tumors are larger than benign tumors less uniform in shape and of variable attenuation’s on CT scans [64]. Adenomas are usually asymptomatic. They occur most commonly in the duodenum. SI adenomas are single, usually in older patients but occasionally multiple adenomas are present especially in those with variations of familial adenomatous polyposis or Gardner’s syndrome [65]. On barium studies, they appear as either sessile or pedunculated intraluminal defects (Fig. 4). The commonest clinical presentation of lipomas is with obstruction [40]. Barium contrast studies demonstrate a sharply demarcated, often pedunculated tumor that tends to conform the contour of the SI lumen. CT can establish the diagnosis of SI lipoma by showing its attenuation values to be consistent with fat (Fig. 5) [12].
In contrast to other benign SI tumors, which are often asymptomatic, 80% of hemangiomas produce significant symptoms [66]. Plain film of the abdomen occasionally will show calcified phleboliths in different locations in the abdomen, a result of normal positional changes of bowel loops. Barium studies rarely outline hemangiomatous polyps and are likely miss the usually shallow elevations, unless the presence of phleboliths draws attention to them [12]. Inflammatory fibroid polyps are usually solitary and they have been regarded as an exuberant host response to an unknown injury [67]. The SI is the second most common site for inflammatory fibroid polyp after gas-
Fig. 4. Adenomatous polyp. A solitary polyp (open arrow) 5 mm in size is seen in pelvic ileum on enteroclysis examination.
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Fig. 5. Lipoma. Abdominal CT section demonstrates a rounded intraluminal mass (arrow) of fatty density representing lipoma.
tric antrum. Patients are generally elderly and the lesions generally occur in the ileum (Fig. 6). They may be pedunculated and may reach a size in excess of 5 cm. Erosions and ulcerations of the polyps are frequent [12]. There are no distinctive features to differentiate it from other mural or intraluminal lesions of the GIT
[68]. Contrast studies may demonstrate a smooth rounded mass in the distal SI, like the other benign SI tumors [12]. Fibromas, lymphangiomas and other benign tumors can also occur in the SI. They cannot be differentiated radiographically from other benign tumors.
Fig. 6. Giant fibroid polyp. Enteroclysis in a case with a known history of Crohn’s disease demonstrates typical bird-beak appaerance of invagination (open arrows) as a result of a giant fibroid polyp (p) in distal ileum.
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6.2. Malignant tumors The usual location of the adenocarcinomas is within 25 cm of the duodenojejunal junction. A patient referred for an upper gastrointestinal series for abdominal pain, vomiting or occult gastrointestinal bleeding should have evaluation not only of the duodenum but also of the proximal loops of jejunum. A dilated proxi-
Fig. 9. Intestinal lymphoma. Diffuse concentric bowel wall thickening in a long segment of jejunum and associated multiple mesenteric lymphadenopathies are present on this abdominal CT examination.
Fig. 7. Adenocarcinoma. Classic ‘apple-core’ appearance (arrow) of adenocarcinoma of the proximal jejunum is displayed on enteroclysis, causing partial obstruction.
Fig. 10. Intestinal lymphoma (constructive form). Constructive narrowing, effacement of the folds and destruction of the mucosal pattern in a short intestinal segment (open arrow) is seen on enteroclysis examination.
Fig. 8. Carcinoid tumor. A constructive segment (open arrow) and resultant prestenotic dilatation due to the desmoplastic reaction of the carcinoid tumor is present on enteroclysis examination. The serosal component of the mass causes extrinsic impression (arrow) on the adjacent intestinal loops.
mal jejunum with retrained fluid observed in this extended upper gastrointestinal examination should alert the radiologist to a possible obstructive neoplasm and should be an indication to continue the procedure as a fluoroscopic SI study [12]. The usual radiologic abnormality of a primary adenocarcinoma of the mesenteric SI on barium examination is the ‘apple core’ lesion (Fig. 7) [69]. This is a short annular, circumferentially narrowed segment with features of mucosal destruction. It is frequently ulcer-
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ated and separated from normal bowel wall above and below it by overhanging edges. The malignant stricture is usually central in position, rigid, and without change of shape during compression [54,70]. Lymphomas or leiomyosarcomas may have a similar appearance, but they exhibit alterations of shape with compression, since they are softer [12]. It has been shown that most of the annular apple core type lesions of the SI are as a
result of metastasis commonly from a carcinoma of the colon [71]. Carcinoids only rarely present as annular lesions. The ulcerating form of adenocarcinoma appears as a short narrow lesion usually with an inconspicuous mostly central ulcer. Polypoid mass that intussuscepts is also a rare manifestation of adenocarcinoma. In their CT presentation adenocarcinomas are proximal solitary soft tissue masses causing lumen nar-
Fig. 11. Intestinal lymphoma (cavitary form). (a) Enteroclysis examination shows a large irregular pelvic cavity filled with contrast material. On both sides of the cavity entering and leaving ileal segments are seen. (b) CT section depicts the large cavity (C) which shows air-contrast levels sealed-off by ileal segments.
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Fig. 12. Intestinal lymphoma (aneurysmatic form). A very rare form of intestinal lymphoma which presents as a huge aneurysmatic dilatation of the jejunum on enteroclysis. The folds are not effaced.
rowing and obstruction [72,73]. The lesions may be heterogeneous in attenuation and show moderate enhancement after intravenous contrast medium administration. Mesenteric extension should be suggested in cases with large mesenteric masses with heterogeneous attenuation and associated asymmetric narrowing of SI wall. Regional lymph nodes, liver, peritoneal surfaces and ovaries may be involved by mesenteric spread [12]. The demonstration by enteroclysis or via a carefully performed fluoroscopic SIFT of a smoothly rounded mucosa elevation of about 5– 10 mm in diameter, located in the distal ileum should always plays a carcinoid tumor at the top of the differential diagnosis. In early carcinoids (B1 cm) that not yet involved mesenteric lymph nodes, resection can be curative [12]. Carcinoid tumor lacks radiodiagnostic features characteristic for it and it is indistinguishable from other lesions such as leiomyoma, lipoma, or adenoma. The presence of one or more additional polyps of similar appearance further supports diagnosis of carcinoid [74]. The mucosa overlying carcinoids can ulcerate and it may be possible to demonstrate a carcinoid ulcer by enteroclysis [12]. CT scans of a mesenteric metastasis in addition to the spoke-wheel arrangement due to the emanating fibrosis show it to contain calcifications in well over half of the cases. Fibrosis, as a result of seratonins desmoplastic reaction, is responsible for the fixation, kinking and angulation seen on the SI series (Fig. 8) and the stellate soft tissue density mass on CT scan examinations [12]. Primary SI lymphomas account for approximately
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5% of all lymphomas and represent about one third of all GIT lymphomas [12]. In contrast to adenocarcinoma and leiomyosarcoma, which tend to produce a focal or segmental lesion, lymphoma of the SI originate at multiple sites and extends along the axis of the SI (Fig. 9) [73]. Secondary GI lymphoma usually affects multiple sites: at autopsy, gross or microscopic evidence of GI involvement has been found in up to 50% of cases of disseminated lymphoma [74]. In both the primary and secondary forms, the stomach is the most commonly involved (51%) followed by the SI (33%) [12]. Most of the non-Hodgkin’s lymphomas are of B-cell type, except for the sprue-related T-cell lymphoma [75]. Hodgkin’s disease account for only about 1% of all malignant lymphomas of the GIT [76]. The principal radiologic presentation of SI lymphoma are; circumferential segmental infiltration (Fig. 10), endo-exoenteric disease with cavitation (Fig. 11), aneurysmal dilatation (Fig. 12), polypoid lesions, mesenteric nodal lymphoma with secondary infiltration of SI (Fig. 13), and the possible transformation of diffuse nodular lymphoid hyperplasia into lymphoma (Fig. 14). The infiltrating form generally displays moderate lumen widening and is the most common radiologic appearance, closely followed by the cavitary form [12]. Among all primary malignant tumors in the SI, leiomyosarcomas account for 9% of the cases. Benign leiomyoma and a leiomyosarcoma cannot be differentiated radiographically. Usually, smooth muscle cell tumors that are large or show significant ulceration are malignant [12]. Most of these tumors are slow growing and are associated with a long period of symptoms. Patients are often anemic due to recurrent melena arising from ulcerated component and may complain of abdominal discomfort or pain. Leiomyosarcomas usually appear as an extrinsic mass displacing SI loops, due to the predominant extraluminal growth pattern. Barium studies demonstrate a deformity of the SI segment from which the tumor originates. Flattening, streching and possible ulceration of the mucosa can be seen. Adjacent loops may adhere to the mass as a result of infiltration or tethering by the considerable saprophytic blood supply [12]. Because of the exoenteric growth type of leiomyosarcomas, the manifestations on barium studies tend to be more subtle than the CT findings. The more characteristic CT pattern of a leiomyosarcoma is that of a bulky lesion, growing exoenterically (Fig. 15) [77]. The soft tissue component of the tumor usually shows significant enhancement following intravenous contrast administration [12]. Liposarcoma, angiosarcoma, and fibrosarcoma of the SI are among those rare tumors of SI reported in the literature. They are indistinguishable from leiomyosarcomas [12].
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Fig. 13. Intestinal lymphoma (mesenteric nodal form). (a) Enteroclysis examination shows widely displaced loop of ileum with effacement in plica circulares; also note mild surrounding segment (arrow). (b) CT section demonstrates large mesenteric nodal mass surrounding the ileal segment.
6.3. Metastatic tumors Tumor cells can spread to the SI through intraperitoneal seeding, hematogeneous dissemination, and extension from an adjacent tumor mass either directly or through lymphatic channels [78,79]. The mechanism of tumor spread influences its radiographic appearance. Metastasis through intraperitoneal seeding is most commonly observed in the pelvic SI loops and ileocecal region. When metastases are deposited on the serosal
surface of a segment of the SI, rounded protrusions toward the lumen of lesions at least 1 cm in diameter can be demonstrated by a carefully performed contrast examination (Fig. 16). The folds may assume a curved appearance at the periphery of metastasis or may be seen stretched and ‘tacked down’. Metastatic infiltration and fixation of folds at the affected bowel edge are accentuated by a divergence of folds toward the unaffected side. Associated fibrous reaction may lead to angulation and tethering of folds [12]. The neoplastic implants, such as gastrointestinal, ovarian and uterine
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Fig. 14. Intestinal lymphoma (nodular form). Diffuse submucosal nodular pattern (open arrow) and a slight dilatation in the jejunum is seen on enteroclysis. The folds are not effaced.
in origin, typically grow in relation to the concave or mesenteric border of bowel loops and can incite fibrosis [79]. CT plays an important role in the radiologic demonstration of metastatic lesions in the mesentery, peritoneal surfaces, and lymph nodes as well as in the bowel wall [12].
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Fig. 16. Peritoneal metastasis. Partial obstruction of the intestinal loops (arrows) in several adjacent segments is seen on enteroclysis secondary to peritoneal metastases (primary over carcinoma).
Malignant lymphoma, bronchial carcinoma, especially large cell type, and breast carcinoma are the most common tumors that metastasize to SI hematogenously, in order of frequency. The early radiologic changes in hematogeneous metastases to SI are usually multiple nodules, seen mostly along the antimesenteric
Fig. 15. Leiomyosarcoma. An extramural growing lobulated-contoured pelvic mass originating from the intestinal wall is seen. The mass contains a punctate calcification (arrowhead) and an umblication (arrow) secondary to superficial ulceration.
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Fig. 17. Malignant melanoma metastasis. A large lobulated-contoured intraluminal mass (arrow) and bird-beak appearance (arrowhead) secondary to invagination is seen on enteroclysis.
border, where the vasa recta arborize into a rich submucosal plexus [12]. Metastases can be seen generally as polypoid masses. Infiltrating ulcerative lesions may be seen as well. The polypoid lesions are more common and tend to be large and multiple and have a worse prognosis [12]. Early melanoma metastases to SI usually exhibit a smooth rounded polypoid lesion of different sizes radiographically. The demonstration on barium examination of a nonobstructing, fairly large intraluminal mass favors the diagnosis of melanoma metastasis (Fig. 17) [12]. This is due to the softness of the highly cellular mass, which contains little stroma. Metastases from lung cancer to SI may be shown as single or multiple discrete intraluminal lesions, either flat or polypoid, which are frequently ulcerated [12].
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