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1 Department of Diagnostic Radiology, Technische Universität München,
Klinikum rechts der Isar, Ismaninger Str. 22, D-81675 München,
Germany.
2 Department of Internal Medicine, Technische Universität München,
Klinikum rechts der Isar, D-81675 München, Germany.
Received May 3, 2001;
accepted after revision January 15, 2002.
Address correspondence to K. J. Hellerhoff.
Abstract
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SUBJECTS AND METHODS. Ninety-five patients were studied with a 1.5-T scanner using a T2-weighted single-slice fast spin-echo sequence. Image quality and diameter of the head, body, and tail portion of the pancreatic main duct, the accessory duct, and the side branches were assessed before and after IV administration of secretin. Diagnoses before and after secretin administration were evaluated in a blinded fashion and correlated to the final diagnoses based on endoscopic retrograde cholangiopancreatography (ERCP), intraoperative results, and clinical follow-up as the reference standard.
RESULTS. In patients with a normal pancreatic duct, the
visualization of all portions of the main pancreatic duct and the accessory
duct was significantly improved with dynamic MR pancreatography (p
0.001). In patients with chronic pancreatitis, the visualization of the
main duct was also significantly improved with dynamic MR pancreatography
(p 0.05). However, the visualization of the minor duct and the
side branches was significantly improved only in patients showing no ductal
stricture (p 0.05), compared with those with ductal stricture
(not significant). The overall sensitivity for the detection of chronic
pancreatitis increased from 77% to 89% using secretin-enhanced MR
pancreatography. A pancreas divisum was found in eight patients before and 13
patients after secretin administration. The overall negative predictive value
of MR pancreatography increased from 84% to 98% after secretin
administration.
CONCLUSION. Improvement in image quality after secretin stimulation increases the diagnostic value of MR pancreatography in patients with a normal or nondilated main pancreatic duct and may obviate invasive procedures such as ERCP.
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The availability of T2-weighted fast spinecho sequences adapted for fast single-shot imaging has reduced the acquisition time to 3 sec, allowing repeated breath-holds for dynamic series [20,21,22]. This sequence has been used in initial studies assessing the utility of dynamic pancreatography after secretin stimulation [23,24,25,26].
IV administration of secretin induces the secretion of fluid and bicarbonate by the exocrine pancreas. Thus, ductal filling is increased, and visualization of the pancreatic tract is improved. In addition, the extent of positive duodenal contrast induced by the drainage of pancreatic fluid via the papilla can be assessed semiquantitatively and may be used for the noninvasive evaluation of the exocrine function of the pancreas.
The purpose of this study was to evaluate the secretin-induced improvement of image quality for the individual parts of the pancreatic duct and to assess the diagnostic value of secretin-enhanced MR pancreatography compared with conventional MR pancreatography.
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The following standards of reference were available: diagnostic endoscopic retrograde pancreatography after MR pancreatography (n = 35), intraoperative findings (n = 4), and clinical follow-up (n = 56) including 10 patients with a second MR pancreatography after 6 months. All follow-up examinations included dynamic studies after secretin administration. For clinical follow-up, the family clinician was interviewed at least 6 months after the examination with standardized questions concerning clinical symptoms (upper abdominal pain, diarrhea, and weight loss), pancreatic enzyme levels, and results of further examinations during the follow-up period. These examinations included transabdominal sonography (n = 11), endosonography of the pancreas (n = 5), and helical CT of the upper abdomen (n = 6).
Imaging Techniques
Patients were studied in the morning after at least 12 hr of fasting. MR
examinations were performed using a 1.5-T scanner (Gyroscan ACS NT; Philips
Medical Systems, Best, The Netherlands) with a phased array surface coil
(Synergy body array coil; Philips Medical Systems). Transverse T2-weighted
images were obtained covering the complete liver and pancreas. A
three-dimensional respiratory-triggered fast spin-echo sequence was applied
with a TR/TE of 2500/120, an echo-train length of 23, a slice thickness of 8
mm, a gap of 0.8 mm, a field of view of 188 x 300 mm, a flip angle of
90°, and a matrix of 116 x 256 pixels. The total acquisition time
for this sequence was 3-4 min, depending on respiratory rate.
MR pancreatography was performed using a T2-weighted single-slice fast spin-echo sequence with 2432/800, a slice thickness of 70 mm, an echo-train length of 256, an interecho spacing of 8.3 msec, a flip angle of 90°, a field of view of 350 x 350, a matrix of 240 x 256, and an acquisition time of 2.4 sec. Five single-shot images were acquired at several coronal angles with steps of 10° from -20° to 20°. The optimal section angle that included the entire pancreatic duct and the papillary region was chosen for the following dynamic series.
Presaturation pulses were used anteriorly and posteriorly to reduce artifacts and to exclude spinal fluid and the renal pelvis. After the IV administration of secretin (Secrelux; Goldham Bioglan, Zusmarshausen, Germany) in a dose of one clinical unit per kilogram of body weight, single-slice image acquisition was repeated every 30 sec during the first 10 min after administration. To reduce artifacts due to fluid in the duodenum and jejunum, we used 150 mL of a negative oral contrast agent (Lumirem; Guerbet, Sulzbach, Germany) applied 10 min before the examination. An antiperistaltic drug was administered to eliminate motion artifacts (Buscopan; Boehringer, Ingelheim, Germany). Thus, the overall examination time was 20 min.
Image Analysis
All 102 MR pancreatograms were analyzed in consensus by two radiologists
who were experienced in biliary and pancreatic MR imaging. Clinical data were
available in all patients. The reviewers were unaware of the endoscopic
retrograde pancreatographic, intraoperative, and clinical follow-up findings.
The analyses of dynamic parameters were performed separately in patients with
normal findings and in patients with chronic pancreatitis.
Image quality before and after administration of secretin was classified semiquantitatively using a five-point score: 1, no delineation; 2, poor; 3, sufficient; 4, good; and 5, excellent delineation. The visualization of the pancreatic duct was classified separately for the main pancreatic duct (head, body, and tail), the accessory duct, and the side branches. In addition, the delay between secretin injection and maximum improvement of image quality was documented. The maximum diameter of the different portions of the main duct was measured before and after secretin administration. The extent of pancreatic fluid secretion was classified using the duodenal filling score described by Matos et al. [26] as follows: grade 0, no fluid signal in the duodenum; grade 1, fluid limited to the duodenal bulb; grade 2, fluid filling up to the genu inferius; grade 3, duodenal filling beyond the genu inferius.
Diagnostic image analysis included the evaluation of the presence of pancreas divisum and other anatomic variants, ductal dilatation, ductal irregularities, strictures, stones, and alterations of side branch morphology.
Chronic pancreatitis was diagnosed on the basis of the Cambridge classification if at least three abnormal side branches or main pancreatic ductal changes with ductal irregularities were present [27]. The diagnoses before and after secretin administration were evaluated separately. We analyzed the single-section images that were obtained before secretin administration without knowing the results of the dynamic series performed after secretin administration. These results were correlated with the final diagnoses on the basis of the previously mentioned reference standard.
Statistical Analysis
The quantitative parameters (5-point score for image quality and size of
main pancreatic duct) before and after secretin injection were compared using
a Wilcoxon's signed rank test. The distribution of the duodenal filling grades
in patients with normal pancreatic ducts and in patients with chronic
pancreatitis was compared using the Mann-Whitney U test. Differences
were considered statistically significant when p was less than or
equal to 0.05. The overall negative prediction (normal or abnormal) and the
sensitivity for the detection of chronic pancreatitis were calculated for MR
pancreatography and secretin-stimulated MR pancreatography. The negative and
positive predictive values of the duodenal filling grade for the presence or
absence of chronic pancreatitis were determined.
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In a number of patients, a combination of diagnoses was present, including
chronic pancreatitis, ductal lithiasis, and an anatomic variant (n =
2); chronic pancreatitis and pancreas divisum (n = 2); chronic
pancreatitis and ductal stricture (n = 6); chronic pancreatitis,
ductal stricture, and ductal lithiasis (n = 1); chronic pancreatitis,
ductal stricture, and pancreas divisum (n = 1); and pancreas divisum
and minor papilla stenosis (n =
2).
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Image Quality
Image quality findings are summarized in
Table 1. The improvement of
image quality in control patients was highly significant for all portions of
the main pancreatic duct and the accessory duct (p 0.001). The
delay between secretin injection and the best image quality was 1 min in 4% of
patients, 2-5 min in 94% of patients, and 6 min in 2% of patients. After this
time, no further improvement of image quality was observed. The normal anatomy
before and after secretin is shown in Figure
1A,1B,1C.
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In patients with chronic pancreatitis, secretin application provided better
depiction of all portions of the main pancreatic duct (p 0.05)
(Figs. 2A and
2B). The visualization of the
minor duct and the side branches was significantly improved in patients with
chronic pancreatitis that showed no ductal stricture (n = 18,
p 0.05) compared with those who had ductal stricture (n
= 8, not significant). In patients with ducts that were more than 5 mm in
diameter before secretin application, no further improvement of image quality
could be observed after secretin administration even for the portions of the
main pancreatic duct. The delay between secretin injection and best image
quality was 1 min in 10% of patients and 2-5 min in 90% of patients. After
this time, no further improvement was observed. The mean delay in the patients
with normal pancreatic ducts was not different from the mean delay in the
patients with chronic pancreatitis (p > 0.05).
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Size of Duct
In the patients with normal pancreatic ducts, the mean size (±SD) of
the pancreatic duct was 2.3 ± 0.4 mm (head), 2.2 ± 0.3 mm
(body), and 1.8 ± 0.4 mm (tail) before secretin; and 2.8 ± 0.6
mm (head), 2.6 ± 0.5 mm (body), and 1.9 ± 0.5 mm (tail) after
secretin. The diameter increase was significant in the head and corpus portion
(p 0.0001) but not in the tail (p > 0.05). In 21
patients with normal findings or anatomic variants on MR pancreatography
confirmed on endoscopic retrograde pancreatography (n = 19) or by
intraoperative findings (n = 2), the diameter of the duct did not
exceed 3 mm before and 4 mm after secretin injection in the head and corpus
portion and 2 mm before and 3 mm after secretin in the tail portion. In 19
patients, the dilatation of the duct before or after secretin application was
considered to be abnormal (dominant stricture in chronic pancreatitis,
n = 7; malignant stricture, n = 2; benign papillary
stenosis, n = 5; diffuse dilation in chronic pancreatitis, n
= 1; and intraductal concrements, n = 4). Eight of these patients had
a normal duct of less than or equal to 3 mm before secretin administration. In
six patients with a duct greater than 5 mm in diameter before secretin
application, no further increase could be observed.
Duodenal Filling
The distribution of duodenal filling grades in the patients with normal
pancreatic ducts and the patients with chronic pancreatitis is summarized in
Table 2. The mean grade was
significantly different between the patients with normal pancreatic ducts and
the patients with chronic pancreatitis (p 0.01). The positive
predictive value of a reduced duodenal filling (grades 0-2) for the presence
of chronic pancreatitis as determined by the reference standard was 58%. The
negative predictive value of a normal duodenal filling (grade 3) was 89%. The
mean delay of the onset of duodenal filling was 2.3 min in patients with
normal pancreatic ducts and 3.4 min in patients with chronic pancreatitis,
with no significant difference between these two groups. Two patients with
normal pancreatic ducts who had prior surgery (total gastrectomy in one case
and Billroth II resection in the other case) were excluded. In these patients,
the extent of pancreatic fluid secretion could not be determined because of
jejunal fluid overlap.
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Diagnoses Before and After Secretin
In 15 (16%) of 95 patients, the primary diagnosis before administration of
secretin was changed after addition of the dynamic series
(Table 3).
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The pancreatic duct was considered normal in 58 patients before and in 50 patients after secretin administration. In eight patients with normal findings before secretin administration, the diagnosis was changed after analysis of the dynamic series; a pancreas divisum was detected in three patients. All cases were confirmed by endoscopic retrograde pancreatography.
One patient was found with a duodenal loop of the accessory duct with orthogonal overlay of accessory duct portions mimicking a small pancreatic pseudocyst. Secretin-enhanced studies allowed the identification of the minor duct including the looped portion. Clinical follow-up of this patient showed no symptoms after 1 year.
In three patients, ductal alterations and side branches indicating early chronic pancreatitis could be depicted during the dynamic series. In one of these patients, ductal irregularities and side branches in the tail portion of the main duct were visualized in secretin-enhanced MR pancreatography. Recurrent episodes of pancreatitis appeared during the follow-up. This patient underwent endoscopic retrograde cholangiography five times during the follow-up period with several stent implantations because of distal choledochal stenosis that was attributed to chronic pancreatitis. The cannulation of the pancreatic duct failed three times. Follow-up MR pancreatography showed the same lesions as in the first examination. The second patient presented with upper abdominal pain and reduced exocrine function evaluated by the duodenal secretin test. In secretin-enhanced MR pancreatography and in follow-up MR pancreatography, ductal irregularities were seen in the head and corpus portion and dilated side branches in the head portion of the duct. Dynamic MR pancreatography and follow-up MR pancreatography of the third patient showed diffuse ductal dilatation with a diameter of 5 mm after secretin administration and irregularities over the entire duct.
In one patient, marked ductal dilatation in the head portion that occurred after secretin administration was interpreted as papillary stenosis; clinical follow-up of this patient showed persistent postprandial upper abdominal pain, and follow-up MR pancreatography after 6 months confirmed the prior diagnosis of papillary stenosis (Fig. 3A,3B).
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Among the patients with normal findings after secretin administration, one patient was found with a false-negative result after secretin application. In this patient with recurrent episodes of pancreatitis, the ductal morphologic findings were considered normal even after secretin administration with MR pancreatography. Clinical follow-up, however, showed persistent increased amylase and lipase levels and the patient reported upper abdominal pain. Endosonography performed 6 months after MR pancreatography showed ductal irregularities and parenchymal calcifications indicating chronic pancreatitis.
Thus, the overall negative prediction (normal or abnormal) was 84% on conventional MR pancreatography and 98% on dynamic MR pancreatography.
A pancreas divisum was found in eight patients before and in 13 patients after secretin administration. Five cases of pancreas divisum could only be detected after secretin administration. All of these were confirmed by endoscopic retrograde pancreatography (Table 3).
Chronic pancreatitis was found in 20 patients before and in 23 patients after secretin application. In three patients, chronic pancreatitis was diagnosed on the dynamic series but not on conventional MR pancreatography. The diagnosis was confirmed by clinical follow-up and follow-up MR pancreatography in all three patients. In three patients, ductal patterns of chronic pancreatitis were not detected on both conventional and dynamic MR pancreatography; in one patient with pancreas divisum, endoscopic retrograde pancreatography showed irregularities of the ventral duct. In one patient, endoscopic retrograde pancreatography depicted dilated and altered side branches in the corpus portion of the main duct. The third patient, who was mentioned previously with recurrent episodes of pancreatitis, increased enzyme level, abdominal pain, and chronic pancreatitis was diagnosed on follow-up endosonography with main ductal irregularities and parenchymal calcifications. Thus, the sensitivity for the diagnosis of chronic pancreatitis was 77% with conventional and 89% with dynamic MR pancreatography.
A ductal stricture (n = 3) or papillary stenosis (n = 3) was shown in eight patients before and in 14 patients after secretin administration. In six patients in whom stricture or papillary stenosis was not detected with conventional MR pancreatography, two of three patients with a history of chronic pancreatitis underwent endoscopic retrograde pancreatography, and a ductal stricture was confirmed in both (Fig. 4A,4B,4C). The three patients with papillary stenosis detected only in secretin-enhanced studies were followed up clinically and by a second MR pancreatography after 6 months. All these patients showed intermittent post-pradial upper abdominal pain and recurrent slight increase of pancreatic enzyme levels. Follow-up MR pancreatography after 6 months showed marked dilatation of the main pancreatic duct exceeding 5 mm after secretin administration but no ductal alterations indicating chronic pancreatitis.
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In four patients with chronic pancreatitis, intraductal stones were found on MR pancreatography. All of these were also detected with conventional MR pancreatography.
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Initial reports assessing dynamic MR pancreatography after secretin stimulation showed a significant improvement of image quality of the normal pancreatic duct [24,25,26]. The results of our study correspond to previous studies that showed a significant improvement of visualization of the main pancreatic duct after secretin administration. The accessory duct could be detected in 38% of the patients with normal pancreatic ducts in the dynamic series, which is comparable with the results of endoscopic retrograde pancreatography (44%) [28].
Although improvement of image quality of the main pancreatic duct was less substantial in patients with chronic pancreatitis, it was still statistically significant. Nicaise et al. [25] and Manfredi et al. [24] found no significant changes, most likely because of the higher number of patients with advanced chronic pancreatitis and ductal strictures in their study population.
The visualization of side branches was significantly improved in patients with chronic pancreatitis but only if the patients with ductal strictures were excluded. We conclude that the visualization of side branches during the dynamic series is not induced by ductal strictures but is a typical feature of chronic pancreatitis itself. In patients with a duct of more than 5 mm in diameter before secretin administration, secretin should be omitted because no change of image quality after administration was found. The delay between secretin injection and the best image quality did not exceed 6 min in either group.
To our knowledge, until now no reliable reference data for the diameter of the normal pancreatic duct on MR cholangiopancreatography before and after secretin administration have been established. In our study, 21 patients had normal findings on MR pancreatography that were confirmed by either endoscopic retrograde pancreatography or intraoperative results. In this subpopulation, the duct did not exceed 3 mm before and 4 mm after secretin administration in the head and body of the pancreas. The diameter of the tail portion did not exceed 2 mm before and 3 mm after secretin administration.
Matos et al. [26] found mildly reduced duodenal filling (grade 2) corresponding to mild morphologic changes of chronic pancreatitis on endoscopic retrograde pancreatography in a small patient population. They concluded that a reduced filling grade might represent early chronic pancreatitis. In our study, the duodenal filling grade was significantly higher in patients with normal ducts than in patients with chronic pancreatitis compared with the study population by Matos et al. However, the positive predictive value of a reduced duodenal filling for the presence of chronic pancreatitis was low (58%) in our study because in a number of patients, reduced duodenal filling was not correlated with morphologic ductal changes; in five of 20 patients with normal findings confirmed on endoscopic retrograde pancreatography, a mildly reduced filling (grade 2) was observed. In one patient with normal findings confirmed on endoscopic retrograde pancreatography, the duodenal filling grade was substantially reduced (grade 1). In four of 26 patients with chronic pancreatitis duodenal filling, grade 3 was observed resulting in a negative predictive value of a duodenal filling grade 3 of 89%.
Several authors previously described discrepancies between morphologic and functional changes detected in patients with chronic pancreatitis [29,30,31]. Thus, exocrine insufficiency may precede morphologic changes of the duct in chronic pancreatitis, whereas in some cases, morphologic changes of the duct after acute pancreatitis may be falsely diagnosed as chronic pancreatitis.
In a recent study by Cappeliez et al. [32], duodenal filling grades correlated well with pancreatic exocrine function determined by an intraductal secretin test. In that study, the positive and negative predictive values of a reduced filling grade for reduced exocrine function were 76% and 84%, respectively. In accordance with our results, Cappeliez et al. found no clear relationship between the severity of morphologic ductal changes in chronic pancreatitis and the duodenal filling grade representing the exocrine function of the pancreas.
Because endoscopic retrograde pancreatography and secretin stimulation tests are both invasive and time-consuming procedures, MR pancreatography after secretin stimulation is potentially useful for the assessment of both morphologic and functional changes during a single noninvasive procedure.
In our study, the diagnosis was changed after secretin administration in 15 (16%) of 95 patients. The normal size and shape of the duct in eight of 58 patients before secretin application were classified as abnormal or as having an anatomic variant in the dynamic series. The overall negative predictive value increased from 84% in conventional MR pancreatography to 98% using dynamic MR pancreatography. Thus, the findings of the secretin dynamic studies confidently showed that patients with suspected pancreatic disease did not have the disease, which may prevent the need for ERCP.
Pancreas divisum is the most common pancreatic anomaly, with an incidence of 5-10%. The clinical impact of pancreas divisum remains a matter of debate. Some authors have reported a higher prevalence of pancreas divisum in patients with recurrent acute pancreatitis and related these findings to higher intraductal pressures due to the relatively small orifice of the minor papilla [33]. One large study, however, could not confirm these findings [34]. In our study, a pancreas divisum was detected in eight of 95 patients before and 13 of 95 patients after secretin administration. All these cases were confirmed on endoscopic retrograde pancreatography. Corresponding to a recent study by Manfredi et al. [35], we found that these results show a marked increase of diagnostic confidence for the detection of pancreas divisum.
Side branch ectasia is a main feature of early chronic pancreatitis, but it is not reliably depicted on conventional MR pancreatography. Corresponding to the study by Manfredi et al. [35], we found no significant improvement of the side branch visualization after secretin injection in patients with chronic pancreatitis. However, side branch visualization was improved significantly when patients with ductal strictures were excluded. In three patients, abnormal side branch morphology and ductal irregularities indicating chronic pancreatitis were visualized only after secretin administration. Early chronic pancreatitis was diagnosed in the latter cases, and no further strictures or intraductal stones were found obviating therapeutic endoscopic retrograde pancreatography. Thus, clinical follow-up and repeated MR pancreatography were performed after 1 year, and chronic pancreatitis was confirmed in all cases. Using secretin-enhanced MR pancreatography, we found that the sensitivity for the detection of chronic pancreatitis increased from 77% to 89%.
Previous studies using ultrafast spin-echo sequences have reported sensitivities for pancreatic ductal strictures ranging from 75% to 79% [16, 17]. Nicaise et al. [25] described persistent intraductal signal voids after secretin administration in two patients, suggesting substantial obstruction. These strictures were considered to be minor on endoscopic retrograde pancreatography, and no therapeutic interventions were performed. In our series, the dilatation of the upstream pancreatic duct after secretin injection was considered to be the result of a stricture and occurred in three patients with chronic pancreatitis. In two patients, endoscopic retrograde pancreatography was performed. Both strictures were confirmed but were considered nonrelevant for endoscopic treatment. We therefore hypothesize that the presence of ductal dilatation proximal to an obstruction before secretin administration indicates a severe stricture and requires endoscopic therapy. However, low-grade strictures in chronic pancreatitis seen after secretin administration do not require therapeutic intervention, and follow-up with dynamic MR pancreatography in cases of increasing clinical symptoms is sufficient.
A limitation of this study is that endoscopic retrograde pancreatography was not available as a reference standard in all patients. However, because substantial abnormalities can be reliably excluded by secretin-enhanced MR pancreatography, further invasive diagnostic procedures such as endoscopic retrograde pancreatography cannot be justified for ethical reasons.
In summary, our results indicate that patients with severe obstruction of the pancreatic duct due to advanced chronic pancreatitis do not benefit from secretin administration. In patients with normal ducts or pancreas divisum or in patients with chronic pancreatitis without marked ductal dilatation, dynamic MR pancreatography with secretin substantially improves the visualization of all portions of the pancreatic duct system and significantly increases diagnostic confidence.
Acknowledgments
We thank Martina Gildehaus, Gisa Klotzbach, and Josette Hoehn for technical
assistance and support with data acquisition.
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