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Gastrointestinal Imaging |
1 From the Department of Radiology, University of California San Francisco School of Medicine, PO Box 0628, San Francisco, CA 94143-0628. Received November 25, 1998; revision requested December 30; final revision received June 21, 1999; accepted July 7. Address reprint requests to R.F.T.
| Abstract |
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MATERIALS AND METHODS: Twenty-eight patients clinically suspected to have functional islet cell tumors underwent T1- and T2-weighted spin-echo (SE) MR imaging with and without fat suppression, T2-weighted fast SE imaging, and spoiled gradient-echo (GRE) imaging before and after injection of gadopentetate dimeglumine. Sensitivity, specificity, and the best and minimum number of sequences for definitive diagnosis were determined.
RESULTS: MR images depicted proved islet cell tumors in 17 of 20 patients (sensitivity, 85%). Images were true-negative in eight patients with negative follow-up examination results for more than 1 year. Specificity was 100%; positive predictive value, 100%; and negative predictive value, 73%. Among 20 patients with tumor, T1-weighted SE images with fat suppression and nonenhanced spoiled GRE images each showed lesions in 15 (75%); T2-weighted conventional SE with fat suppression, in 13 (65%); gadolinium-enhanced spoiled GRE, in 12 (60%); and T2-weighted fast SE, in seven of 10 patients (70%).
CONCLUSION: MR imaging accurately depicts small islet cell tumors. T2-weighted fast SE and spoiled GRE sequences usually suffice. Gadolinium-enhanced sequences are needed only if MR imaging results are equivocal or negative.
Index terms: Gadolinium Magnetic resonance (MR), pulse sequences, 770.121411, 770.121412, 770.121415, 770.12143 Pancreas, MR, 770.121411, 770.121412, 770.121415, 770.12143 Pancreas, neoplasms, 770.3191
| Introduction |
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Standard cross-sectional imaging methods such as computed tomography (CT) and ultrasonography (US) frequently fail to depict these small lesions, and selective angiography with venous sampling has been the only radiographic method that can be used to pinpoint the location of the tumor within the pancreas (1). More recently, endoscopic US has been used successfully (2,3) but is an invasive and costly method that cannot be used to assess the entire pancreas.
Intraoperative US can be used to confirm pancreatic lesions suspected or demonstrated with radiographic methods (4). With sensitivity close to 100% when combined with intraoperative palpation, intraoperative US greatly assists the surgeon. Nevertheless, a reliable preoperative method would be useful both to plan definite treatment and to avoid exploratory laparotomy.
Results of several investigations have shown the value of magnetic resonance (MR) imaging for depicting islet cell tumors, but most series were small (511) or retrospective (12). We undertook a prospective investigation in 28 consecutive patients to determine (a) the sensitivity and specificity of MR imaging for depicting functional islet cell pancreatic tumors of 2 cm or less in diameter, (b) the best MR imaging sequences, and (c) the minimum number of sequences needed for a correct and efficient diagnosis.
| MATERIALS AND METHODS |
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Symptoms and laboratory test results indicating insulinoma included the Whipple triad (fasting hypoglycemia, symptoms of hypoglycemia, and immediate relief after intravenous glucose administration) and fasting serum glucose levels of less than 2.8 mmol/L for men and less than 2.5 mmol/L for women. In most patients, increased proinsulin and C-peptide levels also were obtained.
Symptoms and laboratory test results indicating gastrinoma were watery diarrhea or steatorrhea, acid hypersecretion (basal gastric acid output > 15 mmol/h), and a fasting serum gastrin level of more than 200 pg/mL (95.4 pmol/L).
Symptoms and laboratory test results indicating vipoma were watery diarrhea (stool volume
3 L/d), hypokalemia, achlorhydria, and profound weakness.
Exclusion criteria were lesions more than 2 cm in diameter, multiple lesions, or metastatic disease from the islet cell tumor.
A total of 30 consecutive patients suspected to have functional islet cell tumor of the pancreas on the basis of clinical examination findings were examined with MR imaging. Because inclusion criteria limited islet cell tumors to a maximum diameter of 2 cm, two patients with gastrinomas of 3 and 4 cm in diameter were excluded from the final analysis. One of these two patients also had metastatic disease to the liver.
None of the remaining 28 patients had evidence of metastatic disease or of multiple endocrine neoplasia (MEN) type I syndrome. The final group of 28 patients consisted of 17 women and 11 men, with a mean age of 48 years (age range, 1882 years).
Surgical resection of a pancreatic adenoma was performed in 19 of 28 patients. Histopathologic results were used to confirm insulinoma in 17 patients and gastrinoma in two patients. One patient refused surgery but had persistent symptoms of hyperinsulinism for more than 1 year. Two of the 19 patients had undergone prior resection of an insulinoma. One patient's insulinoma recurred at the site of the previous resection, and the other patient's insulinoma reappeared in another location in the pancreas 10 years after removal of the first insulinoma. The size and location of surgical and pathologic findings were carefully compared with MR imaging findings.
In three patients whose initial clinical presentation suggested insulinoma, results of follow-up studies during 1 year showed normal blood glucose, proinsulin, and C-peptide levels. In another three patients suspected to have gastrinoma and in two other patients suspected to have vipoma who had minimally abnormal initial blood test results, results of clinical follow-up examination, of laboratory tests (absence of elevated vasoactive intestinal polypeptide, gastrin, proinsulin, and C-peptide levels), and of subsequent pancreatic biopsy up to 1 year after the initial work-up provided no evidence of a functional islet cell tumor. Negative follow-up study and laboratory data were considered acceptable proof of absence of a functional islet cell tumor, and exploratory surgery was not performed in these eight patients.
Findings of additional work-up in these eight patients indicated severe liver failure, severe peptic disease, and intestinal ischemia as possible causes of the initial clinical presentation. These eight patients were included in the study to assess the false-positive rate of MR imaging when used to depict small islet cell tumors.
MR Imaging Techniques
Initially, 18 patients underwent a tailored MR imaging examination of the pancreas in search of a functional islet cell tumor as part of a clinical protocol approved by the local committee on human research. Informed consent was obtained from each patient after the procedure was explained fully. The two patients who were excluded later from the final analysis belonged to this group. After this initial trial, the protocol was incorporated into routine clinical work-up. Subsequently, another 12 patients underwent MR imaging of the pancreas for suspected islet cell tumor and fulfilled the inclusion criteria for this study.
Patients were asked to fast for 4 hours prior to MR imaging. Before MR imaging began, a catheter was placed in one of the antecubital veins, and 250 mL of 0.9% saline solution was infused during the examination. Orange juice was available between sequences and at the end of the examination to patients who had severe hypoglycemia.
Imaging was performed with a 1.5-T Signa whole-body MR imager (GE Medical Systems, Milwaukee, Wis). In patients who were enrolled in the initial protocol (n = 16), a body coil was applied for radiofrequency transmission and signal reception. Subsequently, the torso phased-array coil became commercially available for the MR imager and was applied for signal reception in the other 12 patients. The torso coil was chosen because of its increased signal-to-noise ratio. The higher signal-to-noise ratio allowed the use of sequence parameters with higher spatial resolution.
The patient was placed in the imager, and a band (16 patients) or the torso phased-array coil (12 patients) was placed firmly across the abdomen to avoid excessive abdominal excursion during breathing. All spin-echo (SE) imaging was performed with spatial presaturation and respiratory motion suppression with high-frequency phase encoding (Exorcist; GE Medical Systems). Spoiled gradient-echo (GRE) imaging was performed with breath holding and flow compensation.
Pulse Sequences
Initially, coronal localizer imaging was performed with a spoiled GRE technique. In the first 12 patients, this technique consisted of fast spoiled gradient-recalled-acquisition in the steady state (GRASS; GE Medical Systems), while fast multiplanar spoiled GRE became available for the examination of the remaining 16 patients. Coronal localizer images were obtained with a section thickness of 10 mm and an intersection gap of 15 mm. All transverse images were selected by using the coronal localizer images and were acquired with a section thickness of 35 mm and a 1-mm intersection gap.
Initially, T1-weighted SE imaging was performed without and then with frequency-selective fat suppression (550/1115 [repetition time msec/echo time msec], two signals acquired; 23 stacks; acquisition time, 4.56.5 minutes). The next two sequences were T2-weighted SE (2,500/30 and 80; two signals acquired; acquisition time, 16.0 minutes), again without and then with fat suppression. In the last 10 patients, T2-weighted fast SE imaging (4,0005,4,0005,000/102 [effective]; two to four signals acquired; acquisition time, 4.06.5 minutes) also was applied. Three patients with proved islet cell tumors refused imaging with the longer conventional SE sequences, and we opted for only the fast SE sequence. The SE images then were analyzed for a pancreatic lesion, and sections were selected for fast spoiled GRE imaging.
Spoiled GRE sequences without and then with intravenous gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) injection were employed during breath holding as fast spoiled GRE (approximately 11/4.2; two signals acquired; flip angle, 70°; acquisition time, 2027 seconds; six sections) in the first 12 patients and as fast multiplanar spoiled GRE (80120/4.2; one to two signals acquired; flip angle, 70°; acquisition time, 1226 seconds) in the subsequent 16 patients.
An echo time of 4.2 msec was chosen because in-phase images have better anatomic resolution, which is necessary to depict small islet cell tumors, than out-of-phase images. Chemical shift artifacts are accentuated during out-of-phase imaging, which results in impaired image quality.
The multisection method is preferable to the single-section technique because it avoids the problem of spatial misregistration due to different depths of breath holds. The patients received careful breathing instructions to ensure adequate coverage of the desired area in the pancreas and to ensure the absence of respiratory motion artifacts.
Gadopentetate dimeglumine was injected rapidly and intravenously as a bolus (0.1 mmol per kilogram of body weight) and was followed by a rapid bolus of 10 mL of isotonic saline solution. The first spoiled GRE images were obtained within the first 2030 seconds after the injection of the gadopentetate dimeglumine bolus, and repeat images were obtained at 1, 2, and 3 minutes.
In the first 12 patients, contrast materialenhanced T1-weighted imaging without and then with fat suppression also was performed after spoiled GRE imaging. These two sequences were eliminated from the protocol after it was determined with initial analysis that they did not add information, and imaging time had to be reduced to improve patient tolerance.
Image Analysis
The radiologists (including N.K.D.) who evaluated the MR images were not aware of the individual surgical or clinical examination results at the time of image interpretation and analysis. However, they knew that all patients presented with signs and symptoms of functional islet cell tumor and were examined specifically to detect or rule out lesions in the pancreas.
To determine the best sequences and optimum combination of sequences for the depiction of functional islet cell tumors of the pancreas, images obtained with each sequence were first analyzed visually, before contrast-to-noise ratio (CNR) (signal intensity differencetonoise ratio) measurements were performed. For this visual analysis, all images obtained with each sequence in the various patients were printed separately and were mixed randomly by one investigator. Two radiologists first analyzed each image separately in random order, in a consensus reading.
The individual sequences were ranked according to lesion visualization: A ranking of 0 meant that no lesion was seen; 1, a lesion probably was seen; 2, a lesion was seen; and 3, a lesion was well seen.
Subsequently, images obtained with each sequence were rearranged to form complete examinations for each patient and were reread to detect lesions in each patient by two radiologists (R.F.T., U.G.M.L.) who were not involved in the initial analysis. One of the two radiologists (R.F.T.) had more than 20 years experience with abdominal imaging, whereas the other was in the 1st year after an abdominal imaging fellowship.
Results from these two reviewers were compared by using the
statistic to measure interobserver agreement in the diagnosis of functional islet cell tumor of the pancreas. Discrepancies were resolved by consensus to obtain a single MR imaging diagnosis.
The results of MR imaging were then compared with the results of surgery, histopathologic, and/or clinical follow-up studies. The various sequences were classified in decreasing order of sensitivity for depicting or ruling out pancreatic lesions associated with clinical signs and symptoms of a functional islet cell tumor. The morphologic appearance of the islet cell tumors and the enhancement pattern after the administration of gadopentetate dimeglumine were assessed. The combined sensitivity, specificity, and positive and negative predictive values of all MR imaging sequences together were determined.
In the patients with tumors visualized on MR images, in the second analysis, CNR, or signal intensity differencetonoise ratios, were determined: CNR, or S
/N ratio, = (ST SP)/SDN, where S
/N is signal intensity difference to noise, ST is the signal intensity of the islet cell tumor, SP is the signal intensity of the normal pancreas, and SDN is the SD of the signal intensity of background noise.
CNRs were used to quantify lesion conspicuity. By applying commercially available image-evaluation software (ADVANTAGE WINDOWS; GE Medical Systems, Milwaukee, Wis) for the MR imaging system used, MR images were displayed on the system monitor and regions of interest were drawn with an electronic cursor on the tumor, on the normal part of the pancreas, and on a large area immediately ventral to the anterior abdominal wall, with avoidance of bands of vascular pulsation artifacts.
The means and SDs of the signal intensity of pancreatic lesions, normal pancreatic parenchyma, and noise were obtained. CNRs were calculated as absolute values by considering signal intensity only as a detection parameter and not as its positive or negative character.
Gadolinium-enhanced spoiled GRE images showed the best CNRs for the first dynamic (arterial) image obtained after the administration of gadopentetate dimeglumine and showed a rapid decline of enhancement on images obtained at 1, 2, and 3 minutes. For this reason, only the images obtained immediately after injection of the contrast agent were included in the final analysis. CNRs for T2-weighted fast SE imaging were not calculated because only the last 10 patients underwent this examination.
| RESULTS |
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= 0.61). After the consensus reading of all images, the positive predictive value was 100%. In eight patients suspected to have functional islet cell tumors on the basis of clinical examination results, consensus reading yielded no pancreatic lesion and results of several follow-up studies of up to 1 year were negative. MR images in these eight patients were accepted as true-negative, which resulted in a specificity of 100% and a negative predictive value of 73%.
Each of the T1-weighted images obtained with fat suppression and the spoiled GRE images obtained before gadopentetate dimeglumine enhancement showed a lesion in 15 of the 20 patients with proved islet cell tumor (75%). Gadoliniumenhanced spoiled GRE imaging demonstrated the tumor in 12 patients (60%), and T2-weighted SE imaging without fat suppression demonstrated it in 11 of the 17 patients (65%) who underwent MR imaging with this sequence. T2-weighted imaging with fat suppression showed the tumor in 13 patients (65%); T2-weighted fast SE imaging, in seven of the 10 patients (70%) examined with this sequence. In one patient each, the T2-weighted SE images with fat suppression and the gadoliniumenhanced spoiled GRE images were the only images demonstrating a lesion.
Visual analysis of the images obtained with each sequence showed that among the 17 patients with lesions on MR images, in 10 patients, the T1-weighted SE images with fat suppression ranked highest (a ranking of 3) for demonstrating the islet cell tumors, while in four patients, the T2-weighted SE images with fat suppression were best. In two patients in whom the T1-weighted SE images without fat suppression were best, the SE images with fat suppression also were positive, but the lesions were less conspicuous (rankings of 1 and 2) (Fig 2). Postcontrast spoiled GRE images achieved the best result in one patient and were the only images that demonstrated that particular lesion. In four of ten patients in whom T2-weighted conventional SE and fast SE imaging without fat suppression were performed, lesions were depicted on fast SE images that were not seen on conventional T2-weighted SE images.
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In the patient group with insulinoma, the lesion was located in the pancreatic head in eight patients, in the pancreatic body in seven, and in the pancreatic tail in two. In the patients with an insulinoma, the mean largest lesion diameter was 1.4 cm (range, 0.72.0 cm) (Fig 3). Of the two patients with gastrinoma, one had a 2.0-cm lesion in the pancreatic body and one had a 1.0-cm lesion in the wall of the duodenum.
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Table 1 shows the features of the pancreatic lesions on MR images. The adenomas appeared as areas with lower (Figs 3, 4a4c) or higher (Figs 2c, 4d) signal intensity than that of the neighboring normal parenchyma. For some of the sequences, no difference could be observed between the lesion and the normal pancreatic parenchyma. In three patients with islet cell tumors, a substantial amount of collagen was present in the tumor and all three lesions appeared dark on T2-weighted SE conventional images.
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Table 2 shows the calculated absolute values of the CNRs for various imaging sequences in depicting pancreatic adenomas. The values were calculated only for patients with observed and proved tumors. The calculated absolute values demonstrate that for both T1 and T2 weighting, fat-suppressed SE sequences were best, followed by the sequences without fat suppression.
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| DISCUSSION |
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Zollinger-Ellison syndrome is caused by the second most common islet cell tumor, the gastrinoma, and is diagnosed clinically and biochemically. Imaging is needed preoperatively for detecting and localizing insulinomas. In patients with gastrinoma, radiologic evaluation must include screening for metastases, as up to 80% of sporadic gastrinomas show evidence of metastatic disease at the time of discovery of the disease (14). Metastases of insulinoma are rare overall.
According to reports in the literature, the sensitivity of transabdominal US for depicting insulinoma ranges from 19% to 60%, with a mean of 46% (1,5,9,15,16). Endoscopic US provides excellent results in the pancreatic head (sensitivity, 83% [five of six]) but provides poor results in the pancreatic tail (sensitivity, 38% [three of eight]) because of its distance from the stomach (3). Therefore, it is of limited use.
On the basis of study results available from the literature, the sensitivity of CT for depicting insulinoma ranges from 28% to 79%, with a mean of 38%, and is slightly higher for gastrinomas primarily because of their larger size (10,11,1518). It is likely that a dual-phase helical CT protocol would improve the detection rate because it affords optimal depiction of the early and intense enhancement of this hypervascular tumor in the arterial phase. This has been shown anecdotally in two series of seven patients each (19,20), but to our knowledge no data in a large group are presently available in the literature to prove this point.
To our knowledge, at the present time, sufficient data are not available to determine whether somatostatin receptor localization of islet cell tumor with indium 111 octreotide scintigraphy is a reliable method. Preliminary data in 24 patients with biologic and/or histologic evidence of a neuroendocrine tumor showed that results of 111In octreotide scintigraphy were positive in 23 patients (21), but prospective surgical proof could be obtained in only eight of these patients. False-positive and false-negative results have been reported with this method (22).
For insulinoma, angiography is reported to reach a sensitivity between 59% and 80%, while venous sampling reaches a sensitivity between 77% and 94%, with results slightly better for gastrinoma (1,5,9,11,15,16). Our MR imaging sensitivity of 85% for depicting functional islet cell tumors of 2 cm or less in diameter is similar to the sensitivities achieved with those invasive procedures and is superior to most of the MR imaging results reported in the literature (57).
Researchers in some MR imaging studies report a sensitivity of 100%, but the number of patients examined (six to 12 patients) is small (810). For gastrinoma, some study results show MR imaging sensitivities of 20%62% (1517). Our findings in only two patients with gastrinomas of 2 cm or less in diameter do not warrant meaningful statistical analysis. It is very likely that lesions larger than 2 cm would be depicted with MR imaging with a sensitivity of greater than 85%. While the specificity and positive predictive value of MR imaging in our study were excellent, the negative predictive value was only 73%. However, these values should be viewed with caution, as the number of patients without tumor in our series was relatively small.
The superior MR imaging results in our study are based on improved sequence design and better gradients and coils that enable faster imaging sequences, higher signal-to-noise ratios, and superior imaging of early gadopentetate dimeglumine enhancement.
Similar to results in a small series published by Semelka et al (8), our results show that the T1-weighted SE sequence with fat suppression is the best sequence for depicting small islet cell tumors. This is thought to be due to the higher conspicuity of the lesion as compared with the normal part of the pancreas, which has a high hydrogen concentration. In only two of our patients, T1-weighted images with fat suppression displayed the pancreatic lesions with lower conspicuity (Fig 2).
However, in our study, the nonenhanced spoiled GRE images depicted the same number of lesions as the T1-weighted SE images with fat suppression, but with a shorter acquisition time. Because one lesion was shown on only the T2-weighted conventional SE images with fat suppression and because the CNR was much higher with fat suppression than without, we think that the T2-weighted SE images should be obtained with fat suppression.
In the 10 patients in whom T2-weighted conventional SE and fast SE imaging without fat suppression were performed, fast SE images showed lesions in four patients that were not depicted on conventional T2-weighted images. Fast SE imaging without fat suppression had the additional advantage of providing better anatomic detail in the remainder of the abdomen. However, the overall sensitivity was not affected, because T1-weighted imaging demonstrated the lesion in all four patients. Gadolinium-enhanced imaging was needed only if the clinical suspicion for an islet cell tumor was high, but T1- and T2-weighted imaging both failed to demonstrate a lesion or provided insufficient results for a confident diagnosis.
The fact that the two readers agreed on the diagnosis in 82% (
= 0.61) of patients shows that depiction of functional islet cell tumors 2 cm or less in diameter was reliably achieved with MR imaging. Nevertheless, errors in diagnosis occurred slightly more often with the less experienced reader. It appears likely that MR imaging results in patients with functional islet cell tumors are superior when the images are evaluated by a seasoned radiologist with special expertise in abdominal MR imaging.
All depicted islet cell tumors in our 17 patients were small, most 1.5 cm in diameter or less (Fig 3), and the MR images correlated well with the pathology reports and published results of studies on these lesions (23).
Gastrinomas tend to be larger than insulinomas, but our inclusion criteria excluded larger gastrinomas. Both T1 and T2 of islet cell tumors are usually reported to be extremely prolonged, which results in low signal intensity on T1-weighted images and in high signal intensity on T2-weighted images (Figs 2, 3) (16,17,24).
However, as seen in our patients (Table 1), the signal intensity on T2-weighted images may be different, with the result that lesions are either missed or recognized as masses of low signal intensity on T2-weighted SE images (Fig 4). Such a change in signal intensity on T2-weighted images may be due to a substantial amount of collagen present within the tumor. This has also been observed by Mori and colleagues (9). A large amount of fibrous tissue may be caused by long-standing tumor. Because most patients with an islet cell tumor develop symptoms early, when the tumor is still small, it is considered rare to have a substantial amount of fibrous tissue within an insulinoma.
Collagen within the tumor also may be responsible for the variable appearance of the tumor with gadopentetate dimeglumine enhancement. Substantial amounts of collagen were demonstrated during histopathologic analysis in all three patients in our study whose tumors showed low signal intensity on T2-weighted images.
Reasons for missing islet cell tumors include patient obesity associated with irregular breathing that causes poor image quality; inability of the patient to cooperate; very small size of the lesion (6); extensive fibrosis within the lesion (9); and ectopia, such as in the duodenal wall (Fig 1). Ectopic masses are found more often in patients with MEN (14,25), and MR imaging may not be successful in demonstrating these lesions. Our study excluded patients with multiple lesions, some of which may have been ectopic, and/or with metastases.
We have replaced the T1-weighted SE sequence with fat suppression with the nonenhanced T1-weighted spoiled GRE (fast multiplanar spoiled GRASS) sequence. This sequence has the advantages of faster imaging time (1830 seconds vs 4.06.5 minutes) and the absence of breathing artifacts. In our study, images obtained with this sequence showed the lesion in all 15 cases in which T1-weighted SE images with fat suppression depicted the islet cell tumor and, as shown in Table 2, had acceptable CNRs.
On the basis of our results, we recommend T2-weighted fast SE imaging initially, followed by nonenhanced spoiled GRE imaging. The fast SE sequence is preferred over the conventional T2-weighted SE sequence because the acquisition time for the conventional SE sequence is almost 2
times longer than that for the fast SE sequence.
Multisection fast spoiled GRE is superior to the single-section technique (fast spoiled GRE) because it avoids the problem of spatial misregistration related to different depths of breath. If images obtained with these two sequences demonstrate the lesion, no further imaging is needed. If no lesion is shown, fast multiplanar spoiled GRE imaging should be repeated after gadopentetate dimeglumine enhancement, with an immediate or arterial phase (2030 seconds) and a delayed phase (1 and 2 minutes). The delayed phase helps to delineate the normal parenchyma that surrounds the lesion.
If a patient experiences difficulty with the breathing instructions or if spoiled GRE imaging is suboptimal, T1-weighted SE imaging with fat suppression should be used in place of spoiled GRE imaging. It remains to be seen whether use of mangafodipir trisodium (Teslascan; Nycomed, Princeton, NJ), with its enhancement of the normal pancreatic parenchyma, can further improve the depiction of small pancreatic lesions (26).
On the basis of our overall MR imaging sensitivity of 85%, with no false-positive results in consensus readings and with the advancement in fast MR imaging techniques, we recommend MR imaging as the imaging modality of choice for detecting small islet cell tumors, with a T1-weighted spoiled GRE sequence with fat suppression and with a T2-weighted fast SE sequence.
Use of the torso phased-array coil is highly recommended for better delineation of these small tumors. Venous sampling should be reserved for patients with strong clinical suspicion for islet cell tumor but with equivocal or negative MR imaging results. In patients with negative preoperative radiologic examination results but with clear clinical evidence of endocrine disease, intraoperative US and palpation may be the only means of finding the underlying tumor.
Patients with identifiable primary tumor should undergo surgical resection if an insulinoma or gastrinoma is present or debulking in the case of extensive disease due to gastrinoma. At the time of resection, the possibility of additional lesions should be excluded with intraoperative US and palpation.
| Footnotes |
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3 Current address: Radiology Associates, Gwinnett Medical Center, Lawrenceville, Ga.
4 Current address: Radiology Associates of Tarrant County, Fort Worth, Tex.
Abbreviations: CNR = contrast-to-noise ratio GRE = gradient echo MEN = multiple endocrine neoplasia SE = spin echo
Author contributions: Guarantor of integrity of entire study, R.F.T.; study concepts and design, R.F.T.; definition of intellectual content, R.F.T.; literature research, R.C.; clinical studies, R.F.T., P.B.S., N.K.D., U.G.M.L.; data acquisition, N.K.D., P.B.S., R.F.T.; data analysis, R.F.T., R.C., U.G.M.L.; statistical analysis, U.G.M.L., R.C.; manuscript preparation, R.F.T.; manuscript editing and review, R.F.T., U.G.M.L.
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