March 2010, VOLUME 194
NUMBER 3

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March 2010, Volume 194, Number 3

Gastrointestinal Imaging

Original Research

Value of CT Enteroclysis in Suspected Small-Bowel Carcinoid Tumors

+ Affiliations:
1Department of Gastrointestinal Radiology, Hôpital Edouard Herriot, 5 Place d'Arsonval, 69003 Lyon, France.

2Department of Medical Oncology, Hôpital Edouard Herriot, Lyon, France.

Citation: American Journal of Roentgenology. 2010;194: 629-633. 10.2214/AJR.09.2760

ABSTRACT
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OBJECTIVE. The purpose of this study was to evaluate the value of CT enteroclysis in depicting small-bowel carcinoid tumors in symptomatic patients with surgical, histologic, or clinical follow-up findings as a reference standard.

SUBJECTS AND METHODS. At our institution, 44 patients with symptoms of suspected gastrointestinal carcinoid tumors underwent CT enteroclysis. Clinical symptoms were as follows: carcinoid syndrome (n = 3), abdominal pain with diarrhea (n = 24), hypervascular liver metastases (n = 7), subileus condition (n = 1), hypervascular peritoneal lesion (n = 3), abnormal ileal stenosis on optical colonoscopy (n = 3), and follow-up extraintestinal carcinoid lesion (n = 3). Positive CT enteroclysis findings were compared with pathology results after surgical procedures (n = 19). Negative examinations were compared with surgery results (n = 3) or clinical follow-up (n = 22).

RESULTS. CT enteroclysis findings were positive in 19 patients and negative in 25 patients. The sizes of the carcinoid tumors identified were 5–30 mm in axial diameter. These tumors were depicted as focal nodular lesions located in the small-bowel wall or as intraluminal polypoid masses with marked enhancement. Twenty-two patients underwent only clinical follow-up, with a mean clinical follow-up time of 20 months. The overall sensitivity and specificity of CT enteroclysis in identifying patients with small-bowel carcinoid tumors were 100% and 96.2%, respectively. The negative predictive value of CT enteroclysis was 100% and the positive predictive value, 94.7%. Pathologic findings confirmed small-bowel carcinoid tumors in 18 patients.

CONCLUSION. CT enteroclysis should be considered an excellent tool for the diagnosis of the carcinoid tumor before any surgical procedures.

Keywords: carcinoid tumors, CT enteroclysis, oncologic imaging, small bowel

Introduction
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Tumors of the small bowel are rare, accounting for approximately 3–6% of all gastrointestinal neoplasms, although the small bowel covers more than 90% of the intestinal surface [1]. Carcinoid tumors are the most common primary neoplasm of the small bowel (20–30%) [2]. They arise from argentaffin cells in the Lieberkühn crypts and occur most commonly in the distal ileum. The diagnostic strategies used usually depend on the individual clinical presentation and biochemical confirmation. The male-to-female ratio shows a slight predominance in women, and the average age at diagnosis is 64.2 years [3, 4]. Classic carcinoid syndrome occurs in fewer than 10% of patients, and its most typical clinical manifestations include cutaneous flushing and gut hypermotility with diarrhea. Local manifestations (mass, bleeding, obstruction, or perforation) reflect invasion or tumor-induced fibrosis and are often detected incidentally during emergency surgery [5]. In some cases, extensive liver metastases without carcinoid syndrome may occur, reflecting the nonsecretory nature of certain lesions. Biochemical diagnosis is established by the elevation of plasma chromogranin A, serotonin, or urinary 5-hydroxyindoleacetic acid level [5].

The imaging techniques used for the diagnosis of small-bowel carcinoid tumors vary. On barium studies, carcinoid tumors can appear as smooth, solitary, or intraluminal defects but also may exhibit cicatrization, narrowing, and obstruction. Additional studies including enteroscopy, capsule endoscopy, sonography, MRI, somatostatin receptor scintigraphy, and PET may provide useful information.

CT enteroclysis has shown excellent potential in the diagnosis of carcinoid tumors by allowing exploration of the entire small bowel for disease and providing extraintestinal information. The purpose of our prospective study was to evaluate the sensitivity and specificity of CT enteroclysis in detecting small-bowel carcinoid tumor in symptomatic patients with surgery, histologic, or follow-up findings as a reference standard.

Subjects and Methods
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Study Population

From February 2002 to October 2007, CT enteroclysis was performed in 44 consecutive patients who were suspected of having a gastrointestinal carcinoid tumor. Findings on upper gastrointestinal endoscopy and colonoscopy procedures were normal. The study population consisted of 19 men and 25 women (age range, 25–78 years; mean age, 48.2 years). The indication for CT enteroclysis included the presence of carcinoid syndrome (n = 3), abdominal pain with diarrhea (n = 24), hypervascular liver metastases (n = 7), subileus condition (n = 1), hypervascular peritoneal lesion (n = 3), abnormal ileal stenosis on optical colonoscopy (n = 3), and follow-up extraintestinal carcinoid lesion (n = 3).

CT Enteroclysis Protocol

CT enteroclysis was performed using the same protocol by all the radiologists in our department. An 8-French nasojejunal tube (815 NF, Biosphere Medical) was positioned into the duodenojejunal junction with fluoroscopic guidance. Room-temperature water was infused at a rate of 180–200 mL/min using a pressure-controlled pump (NMP V01, Guerbet Group). The pressure was controlled at less than 1,000 mm Hg in all patients. The quantity of water infused through the nasojejunal tube into the small bowel immediately before CT acquisition was 2,500 mL in all patients. Sixty seconds before image acquisition, 15 mL of an antispasmodic drug (tiemonium methylsulfate [Viscéralgine, Laboratoires Organon]) was administered IV to reduce motion artifacts caused by small-bowel peristalsis.

CT enteroclysis was performed with a commercially available MDCT unit (LightSpeed 32 Pro, GE Healthcare) using the following scanning parameters: 32 detector rows and 1.25-section thickness, 120 kVp, 80 mAs, and 0.71-second gantry rotation time (pitch, 0,969; volume CT dose index, 15 mGy). At the start of the procedure, 100 mL of nonionic iodinated contrast material (iomeprol [Iomeron 400, Bracco]) was injected IV through a 20-gauge cannula at a rate of 4 mL/s with an automated power injector. The delay between the start of the contrast material injection and the start of helical scanning was 25 seconds. Images were obtained from the dome of the liver to the lower margin of the symphysis pubis during a single breath-hold. The infusion of water was maintained during image acquisition. A second CT examination was performed 60 seconds after the start of contrast material injection.

Both transverse and coronal images were acquired with the standard window level (50 HU) and width (350 HU) settings that are used in our department for viewing the abdomen and pelvis.

Multiplanar reformatted images were created interactively using an attached workstation (Somatom Volume Wizard, Siemens Healthcare). Axial and coronal images were reconstructed at 3-mm image reconstruction and 2-mm intervals.

Image Analysis

CT enteroclysis images were prospectively interpreted by two experienced gastrointestinal radiologists. Transverse and coronal CT enteroclysis images were analyzed specifically for the presence of small-bowel masses. If a mass or masses were present, the location, number, morphologic characteristics (intramural or polypoid), and contrast enhancement pattern (degree of enhancing) were noted. The CT enteroclysis images were also analyzed for the presence of liver metastasis, mesenteric stranding, and enlarged mesenteric lymph nodes. Liver metastasis was considered to be present if a lesion or lesions were identified in the liver; they could be multiple, solid or cystic. Mesenteric stranding was considered to be present if infiltration of the mesenteric fat was noted. A mesenteric lymph node was considered enlarged when a lymph node was greater than 10 mm in the short-axis diameter.

Standard of Reference

As a standard of reference, we compared positive CT enteroclysis findings with histopathologic findings after surgical procedures (n = 19). Negative examinations were compared with surgical results (n = 3) and clinical follow-up findings (n = 22).

Statistical Analysis

The sensitivity, specificity, positive predictive value, and negative predictive value of CT enteroclysis for the detection of small-bowel carcinoid tumors were calculated. Sensitivity was defined as the true-positive rate—that is, the number of patients with small-bowel carcinoid tumors who were correctly identified as having the disease at CT enteroclysis divided by the number of patients with small-bowel disease who were in our study population (as defined by the standard of reference). Specificity was defined as the true-negative rate—that is, the number of patients without small-bowel carcinoid tumor who were correctly identified as having no disease at CT enteroclysis divided by the number of patients without small-bowel disease who were in our study population. The positive predictive value was defined as the probability that a patient had small-bowel carcinoid tumor when restricted to all patients with small-bowel disease at CT enteroclysis. The negative predictive value was defined as the probability that a patient had no small-bowel carcinoid tumor when restricted to all patients without small-bowel disease at CT enteroclysis. Statistical analysis was performed using commercially available software (SPSS version 10.0, SPSS) for Microsoft Windows. The Youden index was 0.96 and the Yule Q correlation factor was 1.

Results
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CT enteroclysis enabled the detection of a focal gastrointestinal mass in 19 of the 44 patients. Findings from histopathologic examinations were confirmed in 18 cases after surgery (n = 16), biopsy (n = 1), or liver cytology (n = 1), resulting in 18 true-positive cases. Ten patients had a carcinoid mass that manifested as a focal nodular mass located in the small-bowel wall, and eight had a mass that manifested as intraluminal polypoid masses (Figs. 1, 2, 3, 4). The axial diameter of the lesions ranged from 5 to 30 mm, with a mean diameter of 14.8 mm. All the tumors showed marked enhancement after IV administration of contrast material. All patients had a solitary lesion. The distribution of carcinoid tumors was as follows: terminal ileum (n = 16), stomach (n = 1), and Meckel diverticulum (n = 1).

CT enteroclysis helped characterize at the same time extradigestive disease in 11 patients: local desmoplastic reaction in one patient (Figs. 5 and 6), due to mesenteric ischemia and fibrosis caused by release of sero tonin and other hormones from the tumor; enlarged mesenteric lymph nodes in three patients (Fig. 7A, 7B); and liver metastases in seven patients (Figs. 8 and 9).

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Fig. 1 45-year-old woman with carcinoid syndrome. Transverse CT enteroclysis image shows hypervascular enhanced intraluminal mass (arrow) arising in jejunum corresponding to carcinoid tumor.

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Fig. 2 72-year-old man with abdominal pain and diarrhea. Transverse CT enteroclysis image shows focal mural intensely enhanced nodule (arrow), arising in ileum. Histologic study revealed carcinoid tumor.

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Fig. 3 Coronal CT enteroclysis image in 55-year-old man who complained of severe abdominal pain shows carcinoid tumor arising in ileum that manifested as intraluminal polypoid mass (arrow).

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Fig. 4 Carcinoid tumor in 62-year-old woman with abdominal pain and diarrhea. Axial contrast CT enteroclysis image shows hypervascular endoluminal mass (arrow) in small bowel.

Interpretation of CT enteroclysis images resulted in a false-positive finding in one patient: CT enteroclysis showed a solitary endoluminal lesion in the small-bowel wall that was proved with histopathologic findings to be adenoma. There was no extradigestive manifestation.

Negative findings were obtained in 25 patients. Of this group, three underwent surgery and the cause of clinical symptoms was found: appendicitis (n = 1), endometriosis (n = 1), and jejunal polyp (n = 1). Twenty-two patients underwent clinical follow-up with periodic medical examinations for at least 15 months after CT enteroclysis (mean clinical follow-up time, 20 months). All negative findings from CT enteroclysis were considered true-negative.

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Fig. 5 Carcinoid tumor of small bowel in 50-year-old man with sign of obstruction. Coronal CT image shows mesenteric mass (star) with focal calcification (arrow) and tiny dense extensions (arrowheads) inside mesentery (desmoplastic reaction).

The sensitivity of CT enteroclysis in identifying patients with small-bowel carcinoid tumors was 100% (95% CI, 79.3–100%). The specificity was 96.2% (79.6–100%). The negative predictive value of CT enteroclysis was 100% (84.2–100%) and the positive predictive value, 94.7% (73.5–100%).

Discussion
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Carcinoid tumors are the second most common small-bowel malignancy, after adenocarcinoma, and represent approximately 25% of all primary small-bowel tumors (Fig. 10). The 5-year survival rate for patients with a carcinoid tumor of the small bowel is approximately 54% [6]. The survival rate increases to 75% if complete resection of the tumor is performed. If there is a distant metastasis, the 5-year survival rate is less than 20% [6]. Early diagnosis of small-bowel carcinoid tumors continues to pose a significant challenge to the radiologist because these tumors are often small and may be difficult to detect radiographically. The differential diagnosis of small-bowel carcinoid includes adenocarcinoma, gastrointestinal stromal tumor, lymphoma, and mesenchymal neoplasm.

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Fig. 6 Axial contrast-enhanced CT image shows enhancing mass in mesentery (arrow). Note radiating strands of soft tissue extending into mesenteric fat (arrowheads). (Patient shown in this image was not included in our study group.)

Imaging plays a pivotal role in the diagnosis, localization, and staging of carcinoid tumors and in monitoring treatment response. Small-bowel enteroclysis examination shows a submucosal nodule but that nodule may also exhibit thickening, angulation, and fixation of ileal loops as a consequence of mesenteric fibrosis [7]. Therefore, conventional enteroclysis does not depict extraluminal abnormalities and is associated with an increased exposure to ionizing radiation. MRI and MR enteroclysis can be performed to detect intra- and extraluminal small-bowel disease. However, dyspneic patients are excluded because respiratory motion artifacts may compromise MR image detail. Furthermore, the spatial and temporal resolutions of MRI are inferior to CT and subtle small-bowel lesions may not be detected [8].

Capsule endoscopy provides a more complete endoscopic evaluation of the small bowel. The main advantages of capsule endoscopy include relatively low risk for the patient, an absence of radiation, and minimal patient discomfort. However, lesion localization and evaluation can be difficult with capsule endoscopy, with no current ability to measure endoluminal masses and to evaluate extraluminal abnormalities [9]. Other disadvantages of capsule endoscopy are that the examination procedure takes a longer time, it cannot be used in patients with an obstruction or stricture, and the cost of the examination is not reimbursed at this time.

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Fig. 7A 66-year-old woman with carcinoid tumor. Axial (A) and coronal (B) CT enteroclysis shows metastatic lymph nodes (arrows).

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Fig. 7B 66-year-old woman with carcinoid tumor. Axial (A) and coronal (B) CT enteroclysis shows metastatic lymph nodes (arrows).

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Fig. 8 40-year-old man with unknown carcinoid tumor. Coronal CT image shows hypervascular liver metastases.

CT enteroclysis is an imaging technique that combines the advantages of enteroclysis and the morphologic imaging capabilities of helical CT. Because of good spatial resolution and the ability to scan in multiple phases of contrast enhancement, MDCT technology affords the opportunity to detect small-intestine lesions. Luminal distention is required for all small-bowel imaging methods because collapsed bowel loops may falsely appear as wall thickening and can hide even large lesions. Conventional enteroclysis is the only method that provides optimal distention of the luminal tract. The results from different series—in particular, the results reported by Orjollet-Lecoanet et al. [10] in 2000, Boudiaf et al. [11] in 2004, Romano et al. [12] in 2005, and Pilleul et al. [1] in 2006—agree with the observation that CT enteroclysis is valuable for the evaluation of patients with a high clinical probability of presenting a small-bowel tumor.

In our study, 44 patients were suspected of having carcinoid tumors. CT enteroclysis was able to detect 18 carcinoid masses. All of these tumors were confirmed with histopathologic findings. To our knowledge, no study in the literature has attempted as we did to evaluate CT enteroclysis in a group of patients suspected of having carcinoid tumor. These tumors showed marked enhancement after IV administration of iodinated contrast material, and in 70% of cases, the mass contained calcification [13]. Other investigators have suggested that the early contrast enhancement pattern at CT can orient a carcinoid tumor and may be helpful to the pathologist when interpreting a biopsy specimen [14]. In our study, CT enteroclysis findings in one patient who had an adenoma were false-positive for carcinoid tumor. This false-positive finding has a negative effect on the statistical results for the detection of small-bowel carcinoid tumors by CT enteroclysis: Sensitivity was 100% and specificity, 96.2%.

CT enteroclysis also showed metastatic disease and local desmoplastic reaction. In our study, the liver was the most common site for disease spread and liver metastases were found in seven patients. An enlarged mesenteric lymph node was found in three patients. Desmoplastic reaction was found in one patient. Characteristically, carcinoid metastases are hypervascular, and most can be detected easily on CT acquired immediately after contrast material administration [15]. Liver metastases usually show moderately intense enhancement during the hepatic arterial phase [15]. Large metastases may show heterogeneous enhancement due to central necrosis.

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Fig. 9 Multifocal carcinoid metastases in 60-year-old woman. Axial CT image shows hypervascular lesions of liver in hepatic arterial phase.

Some authors have suggested that multiplanar reformatting helps to determine the site and level of the tumors and is especially helpful to surgeons [14]. In our study, using sagittal and oblique multiplanar reformations did not provide additional information.

Negative findings were obtained in 25 patients: 22 underwent clinical follow-up and three underwent surgery. All negative findings from CT enteroclysis were considered true-negative.

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Fig. 10 Photograph of mucosal surface of jejunum removed from 56-year-old man shows submucosal nodule corresponding to carcinoid tumor (arrow).

The undeniable disadvantages of CT enteroclysis are the higher dose of radiation, patient discomfort during placement of the enteroclysis catheter, and the impossibility of exploring the lumen's mucosal lining for anomalies. A limitation of our study is the use of clinical follow-up as a standard of reference when CT enteroclysis gave a negative finding, but it may be difficult to justify performing more examinations in patients with resolving symptoms and negative CT enteroclysis findings.

CT enteroclysis is an irradiating examination because the nasojejunal probe is placed with fluoroscopic guidance and because minimally two CT phases are acquired. Wireless capsule enteroscopy detects more small-bowel lesions than CT enteroclysis, but the advantages of CT enteroclysis include evaluation of disease outside the small bowel, which can complement intraluminal endoscopic findings. CT acquisition should be limited particularly in the evaluation of young subjects and women of childbearing age.

In conclusion, CT enteroclysis has the potential to be an excellent diagnostic method for the examination of carcinoid small-bowel tumors. It provides adequate image quality with multiplanar reformations, allows sufficient distention of the entire small bowel, and provides detailed information about small-bowel masses (size, location, and enhancement) and extraenteric abnormalities (liver metastasis, lymph nodes, and peritoneal metastasis).

Address correspondence to I. Kamaoui ().

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