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1 Department of Radiology, Hospital de la Santa Creu i Sant Pau, Universitat
Autònoma de Barcelona, Sant Antoni M. Claret 167, Barcelona 08025,
Spain.
2 Department of Radiology, Diagnosis Médica, Barcelona, Spain.
3 Department of Gastroenterology, Hospital de la Santa Creu i Sant Pau,
Universitat Autònoma de Barcelona, Barcelona, Spain.
4 Department of Surgery, Hospital de la Santa Creu i Sant Pau, Universitat
Autònoma de Barcelona, Barcelona, Spain.
Received January 22, 2004;
accepted after revision April 20, 2004.
Address correspondence to J. Monill
(jmonills{at}menta.net).
Abstract
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SUBJECTS AND METHODS. Twenty patients who underwent pancreatoduodenectomy were evaluated with secretin MR pancreatography. Single-shot fast spin-echo T2-weighted dynamic MR pancreatograms were obtained before and every minute for 10 min after secretin injection. Image analysis included image quality for the visualization of the pancreatic duct and morphologic features of the pancreatic duct (side branches, ductal narrowing, irregular ductal contour, and patency of the anastomotic site). Pancreatic function was assessed using the Van de Kamer method and the fasting blood glucose and oral glucose tolerance tests. Jejunal filling was graded from the lowest amount of filling (grade 1) to normal filling (grade 3) on the last MR pancreatogram.
RESULTS. The visualization of the main pancreatic duct was significantly improved with dynamic MR pancreatography (p < 0.05). The anastomotic site was visualized in 14 patients (70%) on MR pancreatography after secretin administration (p < 0.05). No statistically significant improvement in other morphologic data was seen after secretin administration. The sensitivity, specificity, positive predictive value, and negative predictive value of reduced jejunal filling (grade 1) for assessment of reduced pancreatic exocrine function were 92%, 71%, 85%, and 83%, respectively. The relation between reduced jejunal filling (grade 1) and diabetes was statistically significant (p < 0.05).
CONCLUSION. The administration of secretin improves visualization of the pancreatic ducts and helps in the evaluation of remnant pancreatic function after pancreatoduodenectomy.
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However, it has been difficult to evaluate the remnant pancreatic function postoperatively with biochemical tests. These tests depend on extrapancreatic factors such as intestinal disorders, hepatic function, and renal function. Secretin MR pancreatography has been used to improve depiction of duct morphology and to provide qualitative assessment of duodenal filling [2-6].
The objective of our study was to assess the usefulness of secretin-stimulated MR pancreatography in evaluating morphologic changes and function of the remaining pancreas after pancreatoduodenectomy.
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Histologic diagnoses were pancreatic duct carcinoma in eight patients, carcinoma of the papilla of Vater in four patients, chronic pancreatitis in seven patients, and intraductal papillary mucinous tumor in one patient. The exocrine pancreatic function was evaluated with the quantitative determination of fecal fat by the Van de Kamer method. This test was performed within 4 weeks of secretin MR pancreatography in all patients.
For endocrine pancreatic function, we examined the plasma glucose concentration using the oral glucose tolerance test. An abnormal glycemic response to the oral glucose tolerance test, diagnostic of diabetes, was defined according to the National Diabetes Data Group [7]. In addition, we evaluated the preoperative plasma glucose concentration in all patients and any changes in this parameter postoperatively.
Imaging Technique
Patients were studied in the morning after at least 8 hr of fasting. MRI
examinations were performed using a 1.5-T scanner (Gyroscan Intera, Philips
Medical Systems) with a phased-array surface coil (Synergy body array coil,
Philips Medical Systems).
Coronal single-shot turbo spin-echo T2-weighted dynamic MR pancreatography (TR/TEeff range, 2,690/1,050-1,200; echo-train length, 256; section thickness, 40-50 mm; matrix, 150 x 256; field of view, 250 mm; acquisition time, 2 sec) was performed before and after secretin stimulation.
After IV administration of secretin (Sekretolin, Hoechst) at a dose of 1 U per kilogram of body weight, acquisition of the optimal section was repeated every 30 sec to 10 min. To eliminate the signal intensity from overlapping fluid-containing bowel, 200 mL of a negative oral contrast agent ([ferumoxsil] Lumirem, Guerbet) was administered 5 min before dynamic MRI.
Image Analysis
All 20 MR pancreatograms were analyzed in consensus by two radiologists;
any interpretation discrepancies were resolved by consensus.
The baseline and maximal diameter of the main pancreatic duct and the time to reach maximal diameter were measured. Measurements of the duct were obtained with an electronic caliper on the screen of an independent diagnostic workstation (Gyroscan NT Diagnostic Workstation, Philips Medical Systems). The image quality of the main pancreatic duct before and after secretin administration was classified semiquantitatively using a 3-point score: 1, poor (the main pancreatic duct was difficult to assess); 2, sufficient (the main pancreatic duct was partially visible); and 3, good (the entire main pancreatic duct was visible). Improvement in image quality after secretin stimulation was subjectively assessed using the following 3-point scale: 1, no improvement; 2, slight improvement; and 3, major improvement in the visualization of the pancreatic duct. The delay between secretin injection and maximum improvement of image quality was documented.
Other parameters assessed before and after secretin administration were the patency of the anastomotic site, morphology of the contour of the main pancreatic duct (smooth or irregular), visualization of side branches, and presence of ductal narrowings.
The jejunal filling volume was semiquantitatively evaluated at 10 min and was graded as follows, according to the method of Matos et al. [2]: grade 1 (no secretion or filling limited to the anastomotic jejunal loop), grade 2 (filling between first and second jejunal loops), and grade 3 (filling of the first two jejunal loops or more) (Fig. 1). Grade 1 was considered to represent reduced jejunal filling capacity. Patients in grades 2 and 3 were grouped for statistical analysis. Chronic pancreatitis was diagnosed on the basis of the Cambridge classification [8]. Side branch dilatation was diagnosed when the observer could visualize side branches on MR pancreatography.
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Statistical Analysis
The McNemar test was used to compare the 3-point score for image quality
and the number of patients with side branches, ductal narrowings, anastomotic
sites, and ductal irregularities visualized before and after secretin
stimulation.
Fisher's exact test was applied to compare the jejunal filling grade seen on MR pancreatography with the fecal fat estimation, diabetes, and postoperative change of glucose tolerance.
The sensitivity, specificity, and positive and negative predictive values of the jejunal filling grade seen on MR pancreatography after secretin stimulation for the presence or absence of pancreatic exocrine dysfunction were determined. Differences were considered statistically significant when the p value was less than or equal to 0.05. Statistical analysis was performed using the Statistical Package for the Social Sciences program version 10.0.
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The delay between secretin injection and the best image quality in the group of 12 patients in whom an improvement was observed was between 2 and 5 min in nine patients (75%) and more than 5 min in three patients (25%).
Side branches were detected in 12 (60%) of the 20 patients before the stimulation of secretin, whereas afterward side branches were detected in 14 patients (70%). Ductal narrowing was detected in five patients (25%) before the stimulation of secretin and in nine patients (45%) afterward (Figs. 3A, 3B). The contour of the main pancreatic duct was irregular in 15 patients (75%) on images obtained before and after secretin administration. The improvement after administration of secretin was not significant for these parameters.
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In two patients (10%), side branches could be depicted only during the dynamic series. In both patients, marked ductal irregularities were seen in the tail portion of the duct. Nonetheless, in six (30%) of 12 patients, more side branches were evident after secretin administration.
In two patients (10%), the baseline study suggested the presence of stenosis. Secretin administration showed only an irregularity in the pancreatic duct in both cases, with no stenotic segments (Figs. 4A, 4B).
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Patency of the anastomotic site in the reconstructed jejunum was confirmed visually in 14 patients (70%), with significant improvement (Figs. 5A, 5B).
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Final Diagnoses
In eight patients (40%), ductal patterns of previously undiagnosed chronic
pancreatitis were detected on conventional MR pancreatography before secretin
administration. Of eight patients, five underwent surgery for pancreatic duct
carcinoma and two, for carcinoma of the papilla of Vater. None of these
patients had a history of acute pancreatitis. One patient with a histologic
diagnosis of chronic pancreatitis had undergone a cephalic
duodenopancreatectomy for clinical suspicion of pancreatic neoplasm. Ductal
morphologic features of chronic pancreatitis, which had not been visualized in
CT studies and previous sonography, were detected on postoperative MRI.
In two patients (10%), the primary diagnosis was changed after the administration of secretin. In these patients, secretin MR pancreatography played a useful role in revealing anastomotic stenosis and recurrence of an intraductal papillary mucinous tumor. In one patient with a history of cephalic duodenopancreatectomy due to carcinoma of the papilla of Vater, MR pancreatography after secretin administration suggested stenosis of the pancreatojejunal anastomosis. Persistent dilatation of the pancreatic duct with delayed jejunal filling was observed. In addition, this patient showed signs of chronic pancreatitis with irregularities in the pancreatic duct and progressive hydrographic parenchymal enhancement (acinar filling) (Figs. 6A, 6B, 6C). Endoscopic retrograde pancreatography confirmed stenosis of the pancreatojejunal anastomosis.
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One 78-year-old man had undergone a pancreatoduodenectomy for intraductal papillary mucinous tumor 3 years earlier. Tumor recurrence in the remaining pancreas was suspected from the results of secretin MR pancreatography and was later confirmed surgically.
Ten of 13 patients with a history of neoplastic disease (eight adenocarcinomas and two carcinomas of the papilla of Vater) had morphologic evidence of chronic pancreatitis (nine patients with newly diagnosed disease and one patient with adenocarcinoma and previously diagnosed chronic pancreatitis). All patients with pancreatic adenocarcinoma showed signs of chronic pancreatitis, although only two of four patients with carcinoma of the papilla of Vater presented ductal morphologic abnormalities.
Jejunal Filling
Correlation between jejunal filling grade on MR pancreatography and the Van
de Kamer test and diabetes are summarized in Tables
3 and
4. Jejunal filling was absent
or limited to the anastomotic site (grade 1) in 14 patients (70%) and occurred
in more than the first jejunal loop (grades 2 and 3) in six patients (30%).
The jejunal filling grade was significantly different between the patients
with normal exocrine pancreatic function and the patients with positive
results on the Van de Kamer test. The two patients (10%) with positive
findings on fecal fat estimation in the second group (grades 2 and 3)
presented a jejunal filling grade 2. Two patients (10%) with reduced jejunal
filling (grade 1) showed normal fecal fat estimation.
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The sensitivity, specificity, and positive and negative predictive values of reduced jejunal filling (grade 1) for the presence of exocrine pancreatic insufficiency were 92%, 71%, 85%, and 83%, respectively. No significant difference was seen in the mean delay of the onset of duodenal filling between the patients with normal exocrine pancreatic function and the patients with diminished exocrine pancreatic function. The postoperative plasma glucose concentration and the oral glucose tolerance test were normal in eight patients (40%) and abnormal in 12 (60%). The correlation between MRI jejunal filling grade and diabetes was significant. Glucose tolerance deteriorated postoperatively in six patients (30%), and no changes were seen in 14 (70%). These postoperative changes in the plasma level glucose did not correlate significantly with MRI jejunal filling grade.
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To preserve the morphology and functionality of the pancreatic remnant as much as possible, various techniques for pancreatic resection and anastomotic reconstruction have been described, but no conclusive results have been reached regarding the best surgical procedure [12, 13].
Postoperative follow-up of changes in pancreatic morphology and exocrine and endocrine function is important for optimizing medical treatment and for eventual decisions about using more aggressive (endoscopic or surgical) therapeutic procedures. Proper follow-up and treatment help to guarantee acceptable quality of life for patients undergoing pancreatoduodenectomy [14, 15].
Sonography and CT are not sufficiently sensitive for the early detection of changes in ductal morphology or incipient grades of atrophy. Direct pancreatography, aside from being an aggressive technique, is technically challenging in this group of patients [16].
Matos et al. [2] showed that MR pancreatography after secretin stimulation is useful for the morphologic and functional evaluation of the pancreatic duct. Secretin administration stimulates fluid and bicarbonate secretion by the exocrine pancreas and induces a transitory increase in the diameter of the pancreatic duct, which improves visualization. In addition, the degree of duodenal filling resulting from the drainage of pancreatic fluid can be evaluated semiquantitatively and used as an indirect measure of pancreatic exocrine function [4-6, 17].
Various studies have shown improvement in the image quality of the pancreatic duct in MR pancreatography with secretin stimulation [17-19], with results similar to those obtained by ERCP.
There have been no studies analyzing the improvement of image quality in patients who have undergone pancreatoduodenectomy. The sphincter of Oddi, which in healthy persons is considered to be one of the main factors responsible for transitory dilation of the pancreatic duct after secretin stimulation, is absent after pancreatoduodenectomy [20]. Nonetheless, in our series a significant improvement in image quality was seen in 60% of patients. This shows that even in the absence of increased Oddi sphincter tone, increased pancreatic secretion suffices to distend the pancreatic ducts. In four of eight patients in whom no improvement was observed, the initial pancreatic duct diameter was greater than 4 mm. In these patients, baseline ductal dilatation allowed ductal morphologic alterations to be adequately evaluated, as shown by the series of Hellerhoff et al. [17].
We found no significant differences in the detection of side branches, ductal narrowings, or ductal irregularities using secretin stimulation. Most studies have reported a clear improvement in the detection of side branches, thus facilitating the diagnosis of early chronic pancreatitis. In the series of Manfredi et al. [4], side branches were detected on conventional MR pancreatography in only 4% of patients with suspected pancreatic disease, whereas they were visualized on dynamic MR pancreatography in 63% of patients. MR pancreatography with secretin stimulation also made it possible to precisely evaluate the number and length of the ductal narrowings producing adequate distention of the pancreatic duct distal to the stenosis [19].
The discrepancy between our results and those of other authors is probably due to differences in our study population, which contained a high percentage of patients with morphologic abnormalities indicative of advanced chronic pancreatitis, most of which were already evident on conventional MR pancreatography. Some studies of patient populations of similar characteristics have also failed to detect a significant improvement in the diagnosis of these abnormalities [3, 4].
In our series, however, secretin stimulation enhanced diagnostic confidence in the evaluation of ductal narrowings by excluding two false-positive findings and by visualizing ductal stenosis that had not been visible on conventional MR pancreatography in four patients (20%).
In two patients in our series, side branches were visible only during dynamic MR pancreatography. However, this finding did not influence the diagnosis because other morphologic changes diagnostic of chronic pancreatitis were observed in both cases.
The permeability of the surgical anastomosis is fundamental for conserving exocrine function; stenosis of the surgical anastomosis is associated with postobstructive chronic pancreatitis and atrophy of the exocrine pancreas. This is a frequent complication after pancreatoduodenectomy, and its frequency increases in relation to time from surgery [11]. Early diagnosis of impaired permeability would allow endoscopic or surgical treatment to prevent irreversible injury to the exocrine pancreas. In our study, in agreement with the results of a recently published study [21], dynamic MR pancreatography was useful for functional evaluation of the anastomosis. We were able to directly assess the permeability of the anastomosis in 70% of patients. In one patient in our series, stenosis of the anastomosis associated with signs of chronic pancreatitis was diagnosed and corrected with endoscopic treatment.
Aubé et al. [21] conclude that a direct correlation exists between a major reduction or absence of gastric repletion by pancreatic fluid and the severity of stenosis of the anastomotic site. We believe that, as described in patients not operated on, impaired pancreatic secretion may occur with exocrine insufficiency in the absence of stenosis. However, because it is also reported in patients who did not undergo surgery, we believe that impaired pancreatic secretion may occur with exocrine insufficiency in the absence of stenosis.
Dynamic MR pancreatography made it possible to semiquantitatively evaluate the filling of the anastomosed jejunal loops. Several studies have confirmed the correlation between degree of duodenal filling and pancreatic exocrine dysfunction in patients without surgery [4-6, 17]. Cappeliez et al. [5] reported sensitivity, specificity, and positive and negative predictive values of 72%, 87%, 76%, and 84%, respectively, in the prediction of pancreatic exocrine dysfunction. Our results were somewhat higher, probably because of the larger percentage of patients with advanced chronic pancreatitis in our series. The same factor would explain the significant correlation between the degree of jejunal filling and the presence of diabetes. Clinical studies have established that endocrine insufficiency is associated with pancreatic parenchymal atrophy both in healthy patients and in patients who have undergone pancreatoduodenectomy. Some studies have reported a parallel loss of pancreatic endocrine and exocrine function in the course of chronic pancreatitis [22].
On the basis of our results, this technique represents a valuable test that can be used routinely in the follow-up of morphologic changes and monitoring of exocrine function in postoperative patients. Compared with biochemical tests, this technique provides a more reproducible measure of pancreatic function that is independent of extrapancreatic factors. Furthermore, as a follow-up test of surgical anastomosis, the technique can be helpful in the early diagnosis of anastomotic stenoses, avoiding an irreversible pancreatic injury.
A large number of patients in our series had evidence of advanced chronic pancreatitis; this diagnosis was preoperative in only one patient. The remaining patients had no history of chronic pancreatitis or clinical episodes of acute pancreatitis. Aubé et al. [21] reported similar findings, with 70% of their patients being newly diagnosed with chronic pancreatitis at the time of MR pancreatography. Those authors postulated that inactivation of pancreatic enzymes by gastric acid secretion could be a causative factor in changes leading to chronic pancreatitis. This factor was not present in our patients because all of them had jejunal anastomoses. We believe that the high prevalence of chronic pancreatitis in patients with pancreatoduodenectomy could be attributed to postobstructive changes secondary to the neoplastic process. Histologic studies confirm the presence of signs of chronic pancreatitis in patients with neoplastic obstruction of the pancreatic duct.
Our study had several limitations. First, we did not establish a correlation with ERCP. ERCP involves major technical difficulties in patients with duodenopancreatectomy. In addition, it would not have been ethically justifiable because MRI findings precluded the need for more aggressive therapeutic or diagnostic procedures in most of our patients. The second most important limitation of the study was the use of the Van de Kamer test as the clinical reference for pancreatic exocrine function. The sensitivity of this test in detecting incipient grades of exocrine insufficiency is low. A more precise evaluation of exocrine dysfunction and its correlation with jejunal filling on MR pancreatography with secretin stimulation would require using more expensive techniques like the fecal elastase-1 test. With this technique, the percentage of patients with exocrine insufficiency would probably have been greater, as in the series of Aubé et al. [21], in which 95% of patients with duodenopancreatectomy had exocrine dysfunction of the pancreas. The low sensitivity of the Van de Kamer test may explain why two patients (10%) in our series with jejunal filling grade 1 showed no evidence of exocrine insufficiency.
In conclusion, MR pancreatography after secretin stimulation is an adequate technique for morphologic and functional evaluation of the pancreas after pancreatoduodenectomy. It allows direct evaluation of the surgical anastomosis and a functional study of pancreatic secretion that indirectly assesses pancreatic exocrine function. This technique represents an alternative to the biochemical tests that are routinely used in these patients to monitor pancreatic function and response to treatment. In patients with signs of chronic pancreatitis and no marked ductal dilatation, dynamic MR pancreatography after secretin stimulation improves ductal visualization, thus enhancing diagnostic confidence in the evaluation of ductal abnormalities.
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