Carcinoid Tumors of the Small Bowel: A Multitechnique Imaging Approach
Small-bowel carcinoid tumors are neuroendocrine neoplasms that present unique imaging challenges. In their early stages, the tumors are small and confined to the bowel wall. Small-bowel series and enteroclysis may be more sensitive for detection than CT or MRI. As the tumor grows, extension outside the involved bowel loop may occur, with infiltration of the mesentery and desmoplastic reaction, which results in a characteristic appearance on small-bowel contrast examinations and cross-sectional imaging. In patients in whom there is a high clinical suspicion of carcinoid tumor but inconclusive barium studies or CT, angiography can be performed and may show the submucosal mass because of its vascularity. Alternatively, in this situation, CT angiography may also be used to localize the mass on the basis of its vascularity and in many cases may obviate conventional angiography.
In addition to contrast studies and CT, nuclear medicine techniques using indium-111– or iodine-123–labeled octreotide or iodine-131–labeled metaiodobenzylguanidine (MIBG) are helpful for diagnosing and locating carcinoid tumors and identifying their metastases.
This article reviews the pathophysiology of small-bowel carcinoid tumors and discusses a variety of radiologic examinations that can be used for the detection, staging, and follow-up of patients with these tumors. A detailed discussion of the value of MDCT and CT angiography is included.
Histology
Carcinoid tumors are relatively rare neuroendocrine tumors. They constitute approximately 2% of all gastrointestinal tumors [1]. However, carcinoid tumors are the second most common small-bowel malignancy [1]. Carcinoid tumors belong to a category of tumors called apudomas (amine precursor uptake and decarboxylation tumors) because they arise from endocrine amine precursor uptake and decarboxylation cells that can be found throughout the gastrointestinal tract and in other organs such as the pancreas and the lung. The tumor arises in the wall of the bowel as a submucosal mass that may result in scarring and kinking of the surface (Fig. 1). Microscopically, carcinoid tumors are made up of small round regular cells containing a round nucleus and clear cytoplasm. A prominent nucleolus is often present [2]. Histologic diagnosis also relies on immunohistochemical stains and electron microscopy. The presence of elevated excretion of 5-hydroxyindoleacetic acid (5-HIAA) is suggestive of a functioning carcinoid tumor [3, 4].
Distinguishing benign from malignant carcinoid tumors on the basis of histology alone is often impossible. Documented metastases or local spread to adjacent organs establishes the malignant nature of the tumor. However, the likelihood of metastasis is related to tumor size. For example, the incidence of nodal and liver metastases is approximately 20–30% in patients with carcinoid tumors smaller than 1 cm but increases to almost 60–80% for nodal metastases and 20% for liver metastases when tumors are 1–2 cm [5–7]. In patients with primary tumors greater than 2 cm, the incidence of nodal metastases is 80% and of liver metastases is 40–50% [5–7].
Approximately 85% of carcinoid tumors arise in the gastrointestinal tract and can be classified according to their site of origin [8]. Tumors originating from the foregut develop in the stomach, duodenum, and pancreas; those arising in the midgut develop in the small bowel, appendix, and right colon; and those arising from the hindgut develop in the transverse colon, left colon, or rectum [2, 8]. Carcinoid tumors can be hormonally active and can release vasoactive hormones into the systemic circulation, which is especially common in patients with hepatic metastases.
Clinical Presentation
Carcinoid tumors are characteristically slowly growing tumors that may go unrecognized for many years. The symptoms are often vague, such as intermittent abdominal pain. The diagnosis is typically not made until the patient undergoes exploratory surgery. These tumors most commonly occur in the fifth or sixth decade of life. The average time from the onset of symptoms to the diagnosis exceeds 9 years [15]. In many cases the diagnosis is not suspected until the patient develops carcinoid syndrome, which typically does not occur until the disease has spread to the liver. However, only 10% of patients will develop the carcinoid syndrome, which is more common with tumors of the ileum and jejunum but also occurs with bronchial and other carcinoid tumors.
The carcinoid syndrome consists of such signs and symptoms as secretory diarrhea, telangiectasia, and bronchial constriction. Flushing is a common and characteristic symptom in patients with carcinoid syndrome. For example, patients with midgut carcinoid often describe a flushing of the face and upper trunk that may be provoked by alcohol, foods containing tyramine (blue cheese, chocolate), red sausages, and red wine [15]. The flushing usually lasts only a few minutes but may occur several times a day. In contrast to patients with midgut carcinoid, patients with foregut carcinoids may experience a more intense prolonged flushing accompanied by skin thickening and telangiectasias. The flushing can be attributed to prostaglandins, kinins, and serotonin, which are released in these hormonally active tumors [15]. Other chemicals that may be produced are dopamine, somatostatin, vasoactive intestinal polypeptide, motilin, substance P, and histamine. The diarrhea associated with carcinoid syndrome is typically watery and explosive. Serotonin seems to play a major role in causing the diarrhea, and therefore a serotonin antagonist (methysergide) can be used for treatment [15]. Bronchial constriction can occur, probably as a result of serotonin and bradykinin resulting in wheezing. Treatment with pharmacologic agents may be helpful in such patients.
Patients with carcinoid syndrome may develop cardiac lesions. The incidence of cardiac abnormalities detected on sonography ranges between 60% and 70%. Changes can be observed in both the pulmonary and tricuspid valves and include pulmonary stenosis, tricuspid insufficiency, and tricuspid stenosis [16, 17]. The exact origin of cardiac valvular disease is not known but is thought to result from the release of the various neuroendocrine substances. In addition to valvular disease, enlargement of the right heart and septal contraction irregularities can occur. Treatment is usually a combination of medicine and surgery.
Radiologic Findings
Barium Studies
The radiologic appearance of carcinoid tumors varies depending on their size and location. Almost 50% of carcinoids in the gastrointestinal tract arise in the appendix and 33% occur in the small intestine [18]. The ileum is the most common location for small-bowel carcinoid tumors, followed by the jejunum. Carcinoid tumors arise from the Kulchitsky's cells in the crypts of Lieberkühn. Therefore, they grow as submucosal nodules. At this stage, small-bowel series, and enteroclysis in particular, are usually more sensitive for the detection of the primary tumor than cross-sectional studies [19]. However, even conventional barium studies (small-bowel follow-through) rarely detect primary tumors smaller than 2 cm [20]. Enteroclysis has been shown to be more accurate than small-bowel follow-through for the detection of small-bowel neoplasms [19].
On the small-bowel series or enteroclysis, submucosal carcinoid tumors appear as smooth solitary intraluminal defects, most commonly in the distal ileum. However, this appearance is not specific for carcinoid; other submucosal masses such as leiomyoma, lipoma, submucosal metastasis, or lymphoma could have an identical appearance [18]. When the submucosal carcinoid tumor ulcerates, the appearance of a “target lesion” may be seen on contrast studies. Target lesions can occur in other tumors such as lymphoma, melanoma, metastatic breast cancer, or Kaposi's sarcoma. Because approximately 30% of carcinoid tumors are multicentric, a contrast study may reveal multiple submucosal nodules. As the small intestinal carcinoid grows, extension and thickening of the muscular layers of the wall may occur. On contrast studies, this feature appears as thickening of the wall and mucosal folds [21]. If the tumor extends outside the bowel loop, it can infiltrate the mesentery and result in a desmoplastic reaction. On contrast studies, a desmoplastic reaction will appear as angulation, tethering, and fixation of the involved small-bowel loops [1] (Fig. 2). Retraction of the loops toward the root of the mesentery can also be seen. If an extensive mesenteric component with fibrosis is present, the mesenteric vessels can be encased, resulting in bowel ischemia.
CT
Because primary carcinoid tumors of the gastrointestinal tract are small, they are often difficult to detect on routine CT scans. For instance, in a study by Picus et al. [22] of patients with carcinoid tumors, the primary tumor was identified preoperatively in only two of nine patients. In fact, in four of nine patients, the site of the primary tumors could not be located even at surgery [22]. However, with the introduction of multidetector scanners, which allow thinner collimation and faster scanning, even small primary tumors can sometimes be seen as dramatically enhancing submucosal lesions (Fig. 3A, 3B). Visualization of the enhancing mural mass is improved if water is given as an oral contrast agent and if multiplanar reconstructions or 3D imaging software is used [23] (Fig. 3A, 3B). The combination of the thin (0.5–1 mm) collimation that is possible with MDCT, rapid scanning, and a fast IV contrast bolus may allow visualization of even small submucosal masses because of their increased vascularity.
When a carcinoid tumor is clinically suspected, we routinely perform MDCT using water as an oral contrast agent. Dual-phase (arterial and venous) imaging is performed after the administration of 120 mL of nonionic iodinated contrast agent injected at 2–3 mL/sec. Dual-phase imaging allows optimal visualization of the arteries and veins. In our experience, volume-rendered 3D CT is crucial in these patients to detect small primary masses.
Although CT scans may not always reveal the small primary mass in the wall of the small bowel, CT is an excellent technique to show the mesenteric extension of tumors and liver metastases. Carcinoids that have infiltrated the mesentery have a characteristic CT appearance [24, 25]. On CT, a carcinoid tumor appears as an ill-defined mesenteric mass containing calcification in up to 70% of cases [26] (Fig. 4). The mesenteric mass appears to be spiculated with a stellate pattern [27] (Fig. 5). Occasionally, the tumor may appear cystic. The size of the mass can vary from 1 cm or less to several centimeters. Because of the mesenteric fibrosis and desmoplastic reaction, the mesenteric vessels may be involved, either directly as a result of encasement and narrowing or indirectly as a result of the secretion of neuroendocrine chemicals that can affect the vessel wall. Three-dimensional CT angiography is especially useful in these patients to fully appreciate the mesenteric mass and its relationship to the vessels (Fig. 6), which information is important for surgical planning.
CT with an IV contrast agent nicely shows the encasement or occlusion of mesenteric vessels, which is best appreciated with 3D CT angiography using volume rendering. Thickening and ischemia of the involved small-bowel loops may also be seen as a result of mesenteric vessel encasement (Fig. 5). Although the CT appearance of a mesenteric mass with calcifications and desmoplastic reaction is suggestive of carcinoid tumor, other conditions such as treated lymphoma or retractile mesenteritis can have a similar CT appearance [28].
Carcinoid metastases to the liver have a characteristic CT appearance because of their vascularity [29] (Fig. 7). On early (arterial) phase imaging after the administration of an IV contrast agent, these metastases enhance brightly. On delayed imaging, these lesions may become isodense with the liver parenchyma. Therefore, if metastatic carcinoid tumor is suspected, arterial phase imaging should be performed. In addition to the liver, metastases can occur in the lung, bones, and peritoneum. CT or sonography can be used for guidance if percutaneous biopsy is indicated.
MRI
The literature regarding the MRI appearance of carcinoid tumors is limited. However, a recent article by Bader et al. [8] describes the MRI appearance of primary and metastatic gastrointestinal carcinoids in a series of 29 patients. The primary tumors had two appearances. In several patients, the primary tumor appeared as a discrete mass that enhanced with gadolinium. The appearance of unenhanced T1- and T2-weighted images varied. Most tumors were isointense to muscle on T1-weighted images and either hyperintense or isointense to muscle on T2-weighted images (Figs. 8A, 8B, 8C and 9A, 9B, 9C). In several patients, a discrete mass was not seen, but uniform bowel wall thickening was present. Such wall thickening was isointense on T1- and T2-weighted images and showed enhancement after the administration of an IV contrast agent. At surgery, this area of thickening corresponded to one or more small submucosal nodules.
The MRI appearance of mesenteric nodal extension resembled that seen on CT. In this series, the mesenteric masses ranged between 1.8 and 4 cm and had a spiculated appearance that was isointense to muscle on T1- and T2-weighted unenhanced images. The desmoplastic reaction and stranding could be seen as hypointense strands [8]. Calcification, which is common on CT, cannot be seen on MRI. After the administration of gadolinium, intense enhancement was noted in most patients.
The MRI characteristics of hepatic metastases caused by neuroendocrine tumors have recently been reported. A study by Dromain et al. [30] described signal intensity changes on the unenhanced images and patterns of enhancement after gadolinium administration in 37 patients with 359 hepatic metastases. Most metastases were hypointense on unenhanced T1-weighted images and moderately or strongly hyperintense (close to the signal intensity of fluid) on T2-weighted images [30]. As with CT, on MRI most liver metastases in patients with carcinoid tumor will be hypervascular and are best seen on arterial phase imaging after the administration of gadolinium (Fig. 8A, 8B, 8C). Approximately 10% of metastases were seen only on the arterial phase, according to Dromain et al. During the portal venous phase, many lesions will become isointense and therefore difficult to detect [8]. Larger metastases may show heterogeneous enhancement and even central necrosis. Occasionally, enhancement may be peripheral, with progressive fill-in but without a globular pattern. Delayed enhancement has also been reported [30]. These cases are difficult to differentiate from hematomas, particularly if they are also strongly hyperintense on T2-weighted images (Fig. 8A, 8B, 8C). In such cases, somatostatin receptor scintigraphy or biopsy may be necessary.
MR angiography can be performed in patients with carcinoid tumors to evaluate vascular involvement. As with 3D CT angiography, this information is important for surgical planning.
Angiography
The role of angiography in the diagnosis and localization of carcinoid tumors has decreased significantly during the past decade as cross-sectional imaging and nuclear medicine studies have improved. However, diagnostic angiography may still be used in patients in whom imaging studies are equivocal [28]. Because the primary tumor is well vascularized, the angiogram may reveal a focal blush of enhancement at the site of the primary intramural mass. In patients with carcinoid tumor and mesenteric spread, the mesenteric vessels may appear to be retracted, beading, or tortuous, and in some cases may even be occluded because of the desmoplastic reaction [15]. Liver metastases will appear hypervascular but are typically visualized better on cross-sectional imaging studies such as CT or MRI. Occasionally hormonal assays are performed on subselective portal venous and systemic venous blood samples to help locate the tumor when other tests have failed.
Often conventional angiography can be avoided if good-quality CT or MR angiography is available. CT and MR angiography are much less invasive, use less IV contrast material, and have the ability to visualize the vessels in an infinite number of planes.
Nuclear Medicine
MIBG is a structural analogue to norepinephrine, and 131I-labeled MIBG can be used for the detection of several neuroendocrine tumors such as pheochromocytoma, neuroblastoma, and carcinoid tumors. After MIBG is administered by IV injection, its physiologic uptake occurs in the liver, salivary glands, spleen, heart, and lungs. Excretion occurs predominantly via the kidneys, but limited intestinal secretion also takes place. The use of MIBG for the detection of carcinoid tumor was first described by Fischer et al. [31] in 1984. In a study by Adolph et al. [3] of nine patients with carcinoids, MIBG showed nine of nine intestinal carcinoids, but it was less successful in patients with bronchial (four of six) and thymic (none of two) carcinoid tumors.
Somatostatin itself or its long-acting analogue octreotide can also be used in the diagnosis of carcinoid tumors. These agents bind to somatostatin receptors that are expressed in more than 80% of carcinoid tumors. In a large European study using somatostatin scintigraphy, 90% of carcinoid tumors were detected [32]. Indium-111 octreotide (pentetreotide) has been used to diagnose both gastrointestinal tract carcinoid tumors and liver metastases with a reported sensitivity of 75% and specificity of 100% [33]. The positive predictive value was 100% and the negative predictive value was 63% [33] (Fig. 10). Although these results are impressive, the spatial resolution of nuclear medicine imaging is still limited. The use of positron emission tomography (PET) CT may improve this limitation. Typically, patients with suspected carcinoid tumors undergo both conventional cross-sectional imaging studies (CT or MR) and a nuclear medicine study.
One recent study used whole-body fluorine-18 dopa PET for the detection of gastrointestinal carcinoid tumors [34]. In that study, 17 patients with histologically confirmed carcinoid tumors underwent PET imaging with 18F dopa that resulted in 60 true-positive findings (seven primary tumors, 41 nodal metastases, and 12 distant organ metastases). These results were compared with the results of FDG PET (four primary tumors, 14 nodal metastases, and 11 distant organ metastases) and of somatostatin-receptor scintigraphy (four primary tumors, 27 nodal metastases, and 21 distant organ metastases). The overall sensitivity for 18F dopa PET was 65% compared with 29% for FDG PET and 57% for somatostatin-receptor scintigraphy. Interestingly, morphologic imaging such as CT and MRI was more sensitive for distant organ metastases, whereas 18F dopa PET enabled the best localization of the primary tumor and nodes [34].
Treatment
Surgery may be performed to resect the primary tumor and the mesenteric nodal mass. Surgical resection of the mesenteric mass can be difficult because of the extensive desmoplastic reaction, which may involve a considerable length of small intestine. If too much small bowel is resected, short-bowel syndrome will result. In some patients with isolated liver metastases or metastases localized to a single hepatic segment or lobe, surgical resection may also be attempted.
Although surgical resection of as much tumor as possible is still considered preferable in symptomatic patients with extensive liver metastases, chemoembolization may play a role in relieving symptoms and providing sustained tumor control [35]. The aim of hepatic artery chemoembolization is to control hormone-related symptoms, to inhibit growth, and to improve the chances of patient survival [36]. The technique usually consists of the injection of a mixture of cytotoxic drugs, iodized oil, and Gelfoam (gelatin sponge, Upjohn, Kalamazoo, MI) into the branches of the hepatic artery supplying the tumor. This technique can result in a decrease in 5-HIAA, an improvement of symptoms, and a decrease in size of tumors. In a study by Kim et al. [37] of chemoembolization in patients with metastatic carcinoid tumors, biochemical response was observed in 12 of 16 patients. Partial response occurred in four of 16 patients. After chemoembolization, unenhanced CT is usually performed to confirm Lipiodol (iodized oil, Guerbet, Aulnay-sous-Bois, France) deposition in the targeted lesions. However, hyper-attenuating iodized oil impairs assessment of residual tumor enhancement on contrast-enhanced CT. Iodized oil does not cause signal intensity changes on unenhanced MRI and is difficult to detect [38]. Gadolinium-enhanced MRI can be used to assess treatment response. Enhancing areas in the lesion are presumed to be viable tumor, and lack of enhancement suggests tumor necrosis.
In addition to chemoembolization of liver metastases, radiofrequency ablation has also been used in this patient population. In a recent study by Wessels and Schell [39], three patients with metastatic carcinoid tumors that were resistant to standard hepatic artery embolization with Lipiodol and Gelfoam were treated with radiofrequency ablation. Although the follow-up of these patients was only for a short term (6 months), all the patients realized a decrease in symptoms.
Somatostatin analogues have a role in treatment as well as diagnosis of carcinoid tumors [40]. Octreotide is often used to relieve the symptoms of carcinoid syndrome.
The use of standard chemotherapy agents such as 5-fluorouracil, doxorubicin, and streptozocin is not very successful. In some cases, chemotherapy may be used in combination with surgery, chemoembolization, and somatostatin analogues [41]. Carcinoid tumors are not particularly radiosensitive so radiation does not usually play a role except for the rare treatment of bone metastases.
Conclusion
Small-bowel carcinoid tumors are neuroendocrine neoplasms that present unique imaging challenges. Improvements in CT technology, including the introduction of MDCT scanners and advanced 3D imaging capabilities, have renewed interest in using CT to detect small-bowel malignancies. It is important for the radiologist to be familiar with the CT appearance of carcinoid tumors.
Footnote
Address correspondence to K. M. Horton ([email protected]).
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Submitted: August 21, 2003
Accepted: September 11, 2003
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