Incidental Colonic Focal Lesions Detected by FDG PET/CT

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1 Colonic Focal Lesions Detected by FDG PET/CT Nuclear Medicine Original Research Fabrice Gutman 1,2 Jean-Louis Alberini 1 Myriam Wartski 1 Didier Vilain 3 Elise Le Stanc 3 Farid Sarandi 1 Carine Corone 1 Catherine Tainturier 3 Alain Paul Pecking 1 Gutman F, Alberini J-L, Wartski M, et al. Received August 26, 2004; accepted after revision October 19, Department of Nuclear Medicine, Rene Huguenin Cancer Research Center, 35 Rue Dailly, Saint-Cloud, France Address correspondence to J.-L. Alberini (jl.alberini@stcloud-huguenin.org). 2 Department of Nuclear Medicine, Henri Becquerel Cancer Research Center, Rouen, France. 3 Department of Nuclear Medicine, Hospital Foch, Suresnes, France. AJR 2005; 185: X/05/ American Roentgen Ray Society Incidental Colonic Focal Lesions Detected by FDG PET/CT OBJECTIVE. The aim of this study was to assess the performance of FDG PET/CT for the detection of colonic lesions, especially advanced neoplasms (villous or >10-mm adenomas, carcinomas). Because of 18 F FDG accumulation in adenomatous polyps, PET using FDG can detect early premalignant colorectal lesions. MATERIALS AND METHODS. FDG PET/CT studies performed for a 1-year period in 1,716 consecutive patients with various malignant diseases, except colorectal cancer, were retrospectively reviewed. PET images obtained 1 hr after FDG injection and noncontrast CT images used for attenuation correction were fused for analysis. Of 45 patients showing intense focal colonic FDG uptake, 20 patients (with 21 foci) underwent a colonoscopic investigation, and, when necessary, polyp resection. The intensity of FDG uptake was quantified using the standardized uptake value (SUV max ). RESULTS. The FDG colonic foci were associated with 18 colonoscopic abnormalities in 15 patients, with no colonic abnormality detected in five patients (false-positive [FP] results). Histopathologic findings revealed advanced neoplasms in 13 patients (13 villous adenomas and three carcinomas) and two cases of hyperplastic polyps. A difference in the mean SUV max was found between FP and true-positive colonic FDG foci but was not statistically significant (p = 0.14). CONCLUSION. Presence of a focal colonic FDG uptake incidental finding on a PET/CT scan justifies a colonoscopy to detect (pre-)malignant lesions. The fusion of PET and CT images allows an accurate localization of the lesions. PET/CT is a useful tool to differentiate pathologic from physiologic FDG uptake. olorectal cancer is the second leading cause of cancer-related deaths C in the Western world. However, its mortality can be reduced by the screening of asymptomatic persons over 50 years old [1]. Colonic adenomas are considered a precursor of colorectal cancer [2]; the adenoma carcinoma sequence is an established theory for colorectal cancer [3]. Detection and removal of adenomatous polyps are crucial for prevention and a potential cure. The clinical importance of small adenomas (< 5 mm) is controversial because only a few of them will acquire the additional genetic alterations predisposing to cancer. Advanced adenomas are defined as larger adenomas (> 1 cm) or adenomas with appreciable villous tissue or highgrade dysplasia. Prevention of colorectal cancer is now mainly based on reliable tests able to detect and remove the advanced adenomas before they become malignant [4 6]. PET imaging using 18 FDG (FDG PET) is well accepted in the imaging workup of various malignancies. PET is recognized as a useful tool to manage colorectal cancer and was shown to have an additional value in the detection of colorectal cancer recurrence [7]. The usefulness of FDG PET for incidental premalignant colonic lesion detection has been previously reported [8 11] but to our knowledge, no study has evaluated combined PET/CT for the same purpose. The aim of this retrospective study was to assess the value of PET/CT to detect colonic lesions, especially advanced neoplasms, compared with colonoscopic findings in patients referred for PET/CT studies for different malignant lesions with colonic nodular FDG foci. Materials and Methods Patients We retrospectively analyzed the records of 1,716 consecutive patients who underwent an FDG PET/CT scan for a malignant disease during a 1- year period (October 2002 October 2003) at our center. Our institutional review board does not re- AJR:185, August

2 quire their approval or informed consent for review of patient files and images. Patients with a previous history of colorectal cancer were excluded from analysis. Forty-five patients with PET/CT scan reports mentioning a colonic nodular FDG uptake were selected. In each report conclusion, the possibility of a preneoplastic colonic lesion was stated and a colonoscopy was recommended. Among these 45 patients, 20 patients (12 men, mean age 65 ± 9 [SD] years old) with 21 nodular FDG foci underwent a colonoscopy within 3 months after the PET/CT study. The primary malignancies of these patients were lung carcinoma (n = 7), breast carcinoma (n = 6), carcinoma of unknown primary (n = 3), Hodgkin s disease (n = 1), melanoma (n = 1), pancreatic cancer (n = 1), and ethmoidal cancer (n = 1). Despite a mean follow-up of 7.8 ± 3.5 months and a mail and telephone contact with each patient s referring physician, 25 patients did not undergo a colonoscopy. PET/CT Acquisitions PET/CT studies were performed using a combined PET/CT scanner (Discovery LS, GE Healthcare). Patients were asked to fast for at least 6 hr before FDG injection; their blood glucose levels were determined in capillary blood samples before FDG injection. In our department, the cutoff blood glucose level that contraindicates FDG injection is 8 mmol/l. PET images were acquired 1 hr after injection of 4 5 MBq/kg of FDG on a 2D mode, from the skull to the midthigh, with 5 7 bed positions of 5 min each. CT images were used for attenuation correction and fusion; no contrast medium was used. Helical CT was acquired first with the following parameters: 40 mas, 140 kv, 5-mm section thickness, 0.8 sec per CT rotation, and 22.5 mm/sec table speed. Whole-body CT was performed in a craniocaudal direction. Immediately afterward, PET data were collected in a caudocranial direction. The CT data were resized from a matrix to a matrix to match the PET data to fuse the images. Colonoscopy and Surgery A rectosigmoidoscopy was performed in the five patients who had a focal FDG uptake located within the rectosigmoid on PET/CT fused images. The 15 remaining patients underwent a colonoscopy. All the lesions that appeared suspicious of malignancy were biopsied and removed by polypectomy and/or surgery, and their localization was recorded. Colonoscopy with pathology examination was considered the gold standard in our study. Data and Statistical Analysis Attenuation-corrected and noncorrected PET images, together with the coregistered CT data, were reviewed. Our viewing facilities (entegra workstation, GE Healthcare) included a triangulation tool; coronal, sagittal, and transverse slices visualization; and PET/CT image fusion. The PET/CT image review was performed without knowledge of the colonoscopy results. The FDG uptake pattern was specified as nodular-focal or nodular-multifocal. The colon was divided into five segments on PET/CT images (ascending colon, transversal colon, descending colon, sigmoid, and rectum) for a more precise localization of the FDG uptake, allowing comparison with the colonoscopic findings. A PET/CT result was considered a truepositive (TP) when an FDG focus and a colonoscopic abnormality were situated in the same segment. A false-positive (FP) PET/CT result was defined as a focal FDG uptake without matching colonoscopic abnormality. When the colonoscopy detected premalignant or malignant lesions with no corresponding focal FDG uptake, the PET/CT result was interpreted as false-negative (FN). Per-patient and per-lesion analyses were performed to evaluate the FDG PET/CT positive predictive value for the detection of colonic abnormalities. We focused on the ability of PET/CT to detect advanced adenomas (e.g., adenomas >10 mm in diameter, adenomas with a villous component or moderate to severe dysplasia) and carcinomas. A semiquantitative analysis of FDG activity was obtained by calculating the maximum standardized uptake value (SUV max ) for each focal FDG uptake in the attenuation corrected PET data. The SUV max is a glucose metabolism index derived from the FDG PET data. It represents the ratio of a region of interest uptake to the average whole-body uptake [12, 13]. SUV = Mean ROI activity (MBq/mL) Injected dose (MBq) Body weight (g) Decay factor The SUV max (mean and SE values) was correlated with the different histologic findings using a t test. Our image review also included a record of the colon CT appearances in the region of the FDG uptake, taking into account the peristaltic intestinal motions that could have occurred between the CT and PET data acquisitions. We were specifically looking for the following features: fecal stasis, wall thickening, intraluminal mass, and pericolonic infiltration. Malignancies were suspected with these two latter criteria. Results PET/CT and colonoscopic findings are presented in Table 1. Among the 20 patients included, 19 had one focus of FDG colonic uptake and one patient (patient 19) had two foci on the PET/CT scan. The FDG findings were located within the ascending colon (n = 7), descending colon (n = 3), and the rectosigmoid (n = 11). For three patients (patients 8, 9, and 16), our image review led to a different conclusion from that of the scan report regarding the nature of the FDG focal colonic uptake. The colonic lesion was changed into a physiologic activity because the FDG uptake was located in the colonic lumen without bowel-wall involvement, in an area of fecal stasis. However, we consider this result as obtained after the fact. Consequently, our results are based on the study inclusion criteria as defined initially (that is, the PET/CT scan report), unless stated otherwise. Per-Patient Analysis Among the 20 patients who underwent a colonoscopy, the results were normal in five cases (25%) and showed lesions in 15 patients (75%). In these 15 patients, 18 lesions were found: two benign hyperplastic polyps in the rectosigmoid and 16 advanced neoplasms. The advanced neoplasms consisted of 13 villous adenomas and three adenocarcinomas. The size of the villous adenomas ranged from 4 to 35 mm. The carcinomas were 10, 25, and 48 mm, respectively. The FDG findings matched the colonoscopic abnormalities in 14 patients (TP rate of 70%). In one patient (patient 5), the FDG finding and the polyp detected by the colonoscopy were not located in the same site; thus, the PET finding was considered an FP result. Among the 15 patients who underwent a total colonoscopy, four FN PET/CT results were found in three patients (patients 2, 5, and 6): one 5-mm hyperplastic polyp and three adenomas (two mild to moderate grade dysplasia adenomas of 15 and 20 mm, respectively, located in the ascending colon and rectosigmoid; and one high-grade dysplasia adenoma [20 mm] in the rectosigmoid). Per-Lesion Analysis Fourteen FDG findings matched the colonoscopic abnormalities, which consisted of 10 adenomas, three carcinomas, and one hyperplastic polyp. The adenomas dysplasia was characterized as mild to moderate in six cases and high in four cases. The positive predictive value of PET/CT to detect colonoscopic abnormalities was 67% (14/21) (Table 2). Of the 16 advanced adenomas diagnosed by the colonoscopy, 13 (81%) were detected on the FDG PET/CT scan. 496 AJR:185, August 2005

3 Colonic Focal Lesions Detected by FDG PET/CT TABLE 1: PET/CT and Colonoscopic Findings for 20 Patients P Primary Tumor PET/CT Colonic Foci Colonoscopy TP FP FN Size (mm) Pathology 1 Lung RS RS X 20 HA DC X 35 HA 2 Lung DC RS X 15 MA RS X 20 HA 3 Breast AC X 4 CUP DC DC X 25 C 5 Hodgkin s AC X RS X 5 H 6 Pancreatic AC AC X 20 MA X 20 MA 7 Ethmoidal RS RS X 20 HA 8 Lung AC X 9 Lung DC X 10 Lung RS RS X 20 HA 11 Lung RS RS X 10 MA 12 Lung RS RS X 30 H 13 Breast RS RS X 10 C 14 Breast RS RS X 7 MA 15 CUP AC AC X 48 C 16 Breast RS X 17 Melanoma AC X 18 CUP RS RS X 5 MA AC X 19 Breast RS RS X 15 MA 20 Breast RS RS X 20 MA Note P = patient, TP = true-positive, FP = false-positive, FN = false-negative,rs = rectosigmoid, HA = highgrade dysplasia adenoma, DC = descending colon, MA = mild-to-moderate-grade dysplasia adenoma, AC = ascending colon, CUP = carcinoma of unknown primary, C = carcinoma, H = hyperplastic polyp. Dash ( ) indicates not available because of false-positive PET/CT results. Seven FDG findings situated in the ascending colon (n = 4), descending colon (n = 1), and rectosigmoid (n = 2) did not match any colonoscopic abnormality, and thus, the PET/CT scan results were interpreted as FP (33%). When excluding the three FP lesions that were reassigned as TN findings after review and for which the colonoscopy was negative, the FP rate would have been 22% (4/18). SUV max ranged from 3.1 to 25 (mean value 10.5 ± 6.6). Figure 1 shows the correlation between the SUV max and the histologic findings for four groups: carcinomas, high-grade dysplasia adenomas, mild-tomoderate-grade dysplasia adenomas, and negative colonoscopy. SUV max was 15 ± 11.6 for carcinomas (n = 3), 12 ± 3.7 for high-grade dysplasia adenomas (n = 4), 8.8 ± 4.9 for mild-to-moderate-grade dysplasia adenomas (n = 6), 25 for the benign hyperplastic polyp (n = 1), and 7.1 ± 3.3 in the negative colonoscopy group (n = 7). Excluding the case of the only hyperplastic polyp, we calculated the mean SUV max for the TP and FP results. It was higher in the case of advanced neoplasms (TP, 11.2 ± 6.5, n = 13) than the negative colonoscopy (FP, 7.1 ± 3.3, n = 7) but this value was not statistically significant (p = 0.14). TABLE 2: Comparison of PET/CT Scan and Endoscopy Results (No. of Sites) Colonoscopy PET/CT Scan Positive Negative Total Positive Negative 4 4 Total Regarding the CT findings, a corresponding pericolonic infiltration was found for three FDG foci and an intraluminal mass for six. The colonoscopy was positive for eight of these lesions (two carcinomas, five adenomas, and one hyperplastic polyp) and negative for one. Among the 12 negative CT findings at the site of FDG colonic foci, seven colonoscopies were negative and five positive (one carcinoma, three adenomas, and one hyperplastic polyp). Discussion From the per-patient analysis, it can be inferred that a focal colonic finding on FDG PET/CT should systematically lead to performing a colonoscopy. Considering the perlesion analysis, the main result of our study is that among the 21 FDG findings detected in 20 patients, 13 advanced neoplasms (10 adenomas and three carcinomas) were found. Our results are consistent with two large studies showing that FDG PET is a sensitive tool to detect premalignant lesions [8, 9]. In a series of 3,210 PET scans performed for screening, focal FDG uptake was found in 20 patients and corresponded to 12 villous adenomas, six carcinomas, and two tubular adenomas in the colonoscopy [8]. In another series of 3,000 patients with no previous history of colorectal cancer, 13 focal or multifocal intense FDG uptakes matched 13 abnormalities in the colonoscopy (seven adenomatous polyps and six carcinomas) [9]. In another study, FDG PET had a sensitivity of 74% and a specificity of 84% for the detection of colonic abnormalities in 39 patients referred for a clinical FDG PET scan [10]; however, some patients who had colorectal cancer were included. FDG PET sensitivity to detect adenomas seems to be related to their size, as shown in a cohort of 110 asymptomatic patients who underwent a systematic PET scan and colonoscopy. The TP rate of FDG PET for the detection of adenomas larger than 13 mm was 90%; the FP rate was 5.5% [11]. In our study, the mean SUV max of FDG colonic findings was higher in the TP PET/CT results than in the FP (11.2 ± 6.5 vs 7.1 ± 3.3). We showed that FDG uptake intensity was correlated with the severity of the lesions, although the cutoff value between benign polyps and advanced neoplasms was not clear. We observed that our mean SUV max per category of lesion was higher than that found by Chen et al. [8]. Mean SUV max of carcinomas and adenomas was 5.74 ± 2.26 and 3.56 ± 0.68, respectively. The SUV max of the unique AJR:185, August

4 SUV max Histopathology Fig. 1 Per-lesion standardized uptake value intensity (SUV max ) mean and SD for different colonoscopic findings. = carcinoma (n = 3); = high-grade dysplasia adenoma (n = 4); = mild-to-moderate-grade dysplasia adenoma (n = 6); = negative colonoscopy (n = 7, false-positive FDG PET/CT result). Fig. 2 Intense focal standardized uptake value (SUV max = 15) located in descending colon was associated with colonic wall thickening on fused slices. A 20-mm adenoma with severe dysplasia (arrows) was found in colonoscopy (patient 2). Fig. 3 Intense focal standardized uptake value (SUV max = 12.4) was shown in rectum, corresponding to a 20-mm adenoma with severe dysplasia (arrows) (patient 7). 498 AJR:185, August 2005

5 Colonic Focal Lesions Detected by FDG PET/CT benign hyperplastic polyp detected in our study does not appear consistent with the rest of the SUV max. We could not find a satisfactory explanation for such a discrepancy, which is not in agreement with a previous study that showed no FDG accumulation in 35 hyperplastic polyps [14]. Colonic FDG uptake is relatively frequent on FDG PET and often related to physiologic uptake. The mechanisms of this physiologic activity are unclear: muscular peristaltic activity, presence of lymphoid tissue in the cecum, high concentration of WBCs in the bowel wall, and/or presence within the bowel wall of cells secreting FDG, especially in the case of cecum distention, are hypothesized [15 17]. Physiologic colonic uptake is usually diffused or involves a whole segment, and its intensity is generally moderate. Increased FDG uptake can also be related to inflammation such as enterocolitis [18, 19] or inflammatory bowel disease [20]. Intense FDG uptake with a focal pattern was observed more frequently in the descending colon of constipated patients [21]. In our study, only focal or multifocal FDG findings were considered significant. Despite this criterion, FP results represent 33% (7/21). This rate is lower than the one found by Zhuang et al. [22], who published 9/14 (64%) FP PET scan results for nodular FDG uptake. Nevertheless, the discrepancy can be explained by the higher accuracy of FDG uptake localization allowed by combined PET/CT. CT helps to localize more precisely the FDG findings, particularly when there is a spatial congruence with the bowel wall on the fused images (Figs. 2 and 3). Combining information from anatomic (CT) and functional (PET) imaging techniques improves the scans diagnostic value compared with both techniques taken separately [23, 24]. A recent study [25] showed that combined PET/CT provided more information than the separate interpretation of PET and CT in 99/204 patients and affected the patients management in 14% of the cases. The additional value of combined FDG PET/CT versus FDG PET alone was studied in patients with colorectal carcinoma [26]. FDG PET/CT halved the number of equivocal PET findings and increased the overall correct staging from 78% to 89%. Generally, the CT pattern of carcinoma includes pericolonic infiltration and colonic wall thickening [27], which may be an additional sign of malignancy but is not specific. On the contrary, FDG uptake delineating the bowel lumen on the fused PET/CT images indicates physiologic activity. In our study, an abnormal colonic pattern on the CT slices, such as an intraluminal mass or a pericolonic infiltration, proved to be predictive of a positive colonoscopy for eight of nine lesions. A review of PET/CT slices specifically focused on the colonic FDG uptake led to an improvement in the FP rate (22% vs 33%) (Fig. 4). A proper interpretation of PET/CT implies PET and CT data analysis in combination, keeping in mind the possible inaccuracies of FDG uptake location generated by peristaltic motions occurring between CT and PET image acquisitions. These acquisitions are not simultaneous, and the time interval between them can be as long as min in the abdominal area, generating misregistration. Administering an antiperistaltic agent, such as scopolamine, may be useful in diminishing these motion artifacts [28]. Glucagon has also been used to minimize the smooth muscle spasm and colonic peristalsis [29], but its use remains controversial [30] and it could increase blood glucose level, thus impairing the FDG PET image quality. The use of oral contrast agents can improve PET/CT specificity by a better delineation of intestinal structures, thus allowing a better discrimination between physiologic and abnormal FDG uptake. An overestimation of the FDG activity measured on the attenuation-corrected PET images due to oral contrast agents has been shown [31]. However, this phenomenon does not seem to have much clinical effect: no significant difference in the distribution of intense FDG uptake in the intestinal regions was shown in two groups of 30 patients each [32]. To minimize these artifacts, low-density barium appears suitable for clinical use [33]; administration of a negative oral contrast agent using mannitol is also promising [34]. Avoiding confusion between a colonic FDG finding and physiologic activity in the urinary tract due to the FDG urinary elimination is an additional advantage of PET/CT coregistration. When the cause of an FDG uptake is in doubt, a delayed acquisition step focused on the area, usually the pelvis, can be performed after micturation [35]. Oral or IV contrast agents have to be evaluated to facilitate CT analysis, keeping in mind the artifacts that can be generated by miscalculation of attenuation coefficients and misregistration related to peristaltic motion. Our study showed that colonic neoplasia and particularly advanced incidental neoplasm are suspected when colonic nodular- Fig. 4 Focal colonic FDG standardized uptake value (SUV max = 7) was shown in cecum, with fecal stasis (arrows) on CT image. Colonoscopy was negative (patient 8). AJR:185, August

6 focal FDG findings are detected by PET/CT. Consequently, such findings have to be clearly mentioned in the reports. In a cohort of 20 patients with 21 areas of focal colonic uptake on a routine PET/CT scan, clinically significant lesions were found in 75% of the patients and 67% of the FDG findings. Coregistered PET/CT improves the analysis of colonic FDG uptake by avoiding confusion between abnormal focal uptake and physiologic activity due to fecal stasis, smooth muscular activity, or segmental inflammation. Measurement of SUV max does not allow the differentiation between benign and (pre-)neoplastic lesions, but together with visual analysis, it can decrease the rate of FP results. Detection by PET/CT of high-intensity focal FDG uptake indicative of advanced adenoma should lead to a colonoscopy. References 1. Selby JV, Friedman GD, Quesenberry CP, et al. A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med 1992; 326: Bond JH. Polyp guideline: diagnosis, treatment, and surveillance for patients with colorectal polyps. Practice Parameters Committee of the American College of Gastroenterology. Am J Gastroenterol 2000; 95: Chen CD, Yen MF, Wang WM, et al. A case-cohort study for the disease natural history of adenomacarcinoma and de novo carcinoma and surveillance of colon and rectum after polypectomy: implication for efficacy of colonoscopy. Br J Cancer 2003; 88: Lieberman DA, Weiss DG, Bond JH, et al. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med 2000; 343: Read TE, Read JD, Butterly LF. Importance of adenomas 5 mm or less in diameter that are detected by sigmoidoscopy. N Engl J Med 1997; 336: Pickhardt PJ, Choi JR, Hwang I, et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. N Engl J Med 2003; 349: Flamen P. Positron emission tomography in colorectal cancer. Best Pract Res Clin Gastroenterol 2002; 16: Chen YK, Kao CH, Liao AC, et al. Colorectal cancer screening in asymptomatic adults: the role of FDG PET scan. Anticancer Res 2003; 23: Tatlidil R, Jadvar H, Bading JR, et al. Incidental colonic fluorodeoxyglucose uptake: correlation with colonoscopic and histopathologic findings. Radiology 2002; 224: Drenth JP, Nagengast FM, Oyen WJ. Evaluation of (pre-)malignant colonic abnormalities: endoscopic validation of FDG-PET findings. Eur J Nucl Med 2001; 28: Yasuda S, Fujii H, Nakahara T, et al. 18F-FDG PET detection of colonic adenomas. J Nucl Med 2001; 42: Zasadny K, Wahl R. Standardized uptake values of normal tissues at PET with 2-[fluorine-18]-fluoro- 2-deoxy-D-glucose: variations with body weight and a method for correction. Radiology 1993; 189: Patz EF, Lowe VJ, Hoffman JM, et al. Focal pulmonary abnormalities: evaluation with F-18 fluorodeoxyglucose PET scanning. Radiology 1993; 188: Abdel-Nabi H, Doerr RJ, Lamonica DM, et al. Staging of primary colorectal carcinomas with fluorine- 18 fluorodeoxyglucose whole-body PET: correlation with histopathologic and CT findings. Radiology 1998; 206: Delbeke D. Oncological applications of FDG PET imaging: brain tumors, colorectal cancer, lymphoma and melanoma. J Nucl Med 1999; 40: Engel H, Steinert H, Buck A, et al. Whole-body PET: physiological and artifactual fluorodeoxyglucose accumulations. J Nucl Med 1996; 37: Strauss LG. Fluorine-18 deoxyglucose and falsepositive results: a major problem in the diagnostics of oncological patients. Eur J Nucl Med 1996; 23: Meyer MA. Diffusely increased colonic F-18 FDG uptake in acute enterocolitis. Clin Nucl Med 1995; 20: Kresnik E, Gallowitsch HJ, Mikosch P, et al. (18)F- FDG positron emission tomography in the early diagnosis of enterocolitis: preliminary results. Eur J Nucl Med Mol Imaging 2002; 29: Neurath MF, Vehling D, Schunk K, et al. Noninvasive assessment of Crohn s disease activity: a comparison of 18F-fluorodeoxyglucose positron emission tomography, hydromagnetic resonance imaging, and granulocyte scintigraphy with labeled antibodies. Am J Gastroenterol 2002; 97: Kim S, Chung JK, Kim BT, et al. Relationship between gastrointestinal F-18-fluorodeoxyglucose accumulation and gastrointestinal symptoms in whole-body PET. Clin Positron Imaging 1999; 2: Zhuang H, Hickeson M, Chacko TK, et al. Incidental detection of colon cancer by FDG positron emission tomography in patients examined for pulmonary nodules. Clin Nucl Med 2002; 27: Schöder H, Erdi Y, Larson S, et al. PET/CT: a new imaging technology in nuclear medicine. Eur J Nucl Med 2003; 30: Townsend DW, Cherry SR. Combining anatomy and function: the path to true image fusion. Eur Radiol 2001; 11: Bar-Shalom R, Yefremov N, Guralnik L, et al. Clinical performance of PET/CT in evaluation of cancer: additional value for diagnostic imaging and patient management. J Nucl Med 2003; 44: Cohade C, Osman M, Leal J, et al. Direct comparison of (18)F-FDG PET and PET/CT in patients with colorectal carcinoma. J Nucl Med 2003; 44: Hyun-Jung J, Hyo KL, Soon Jin L, et al. Acute diverticulis of the cecum and ascending colon: the value of thin-section helical CT findings in excluding colonic carcinoma. AJR 2000; 174: Dosda R, Marti-Bonmati L, Ronchera-Oms CL, et al. Effect of subcutaneous butylscopolamine administration in the reduction of peristaltic artifacts in 1.5-T MR fast abdominal examinations. Eur Radiol 2003; 13: Fenlon HM, Nunes DP, Schroy PC 3rd, et al. A comparison of virtual and conventional colonoscopy for the detection of colorectal polyps. N Engl J Med 1999; 341: Morrin MM, Farrell RJ, Keogan MT, et al. CT colonography: colonic distention improved by dual positioning but not intravenous glucagon. Eur Radiol 2002; 12: Antoch G, Freudenberg LS, Egelhof T, et al. Focal tracer uptake: a potential artifact in contrast-enhanced dual-modality PET/CT scans. J Nucl Med 2002; 43: Dizendorf EV, Treyer V, Von Schulthess GK, et al. Application of oral contrast media in coregistered positron emission tomography CT. AJR 2002; 179: Cohade C, Osman M, Nakamoto Y, et al. Initial experience with oral contrast in PET/CT: phantom and clinical studies. J Nucl Med 2003; 44: Antoch G, Kuehl H, Kanja J, et al. Dual-modality PET/CT scanning with negative oral contrast agent to avoid artifacts: introduction and evaluation. Radiology 2004; 230: Miraldi F, Vesselle H, Faulhaber PF, et al. Elimination of artifactual accumulation of FDG in PET imaging of colorectal cancer. Clin Nucl Med 1998; 23: AJR:185, August 2005