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Gastrointestinal Imaging |
1 From the Department of Radiology, Montreal General Hospital, McGill University, Montreal, Canada. Received , 1998; revision requested ; revision received ; accepted , 1999. Supported in part by the French Society of Radiology. Address reprint requests to P.M.B., Department of Radiology, Toronto Hospital, General Division, 200 Elizabeth St, Toronto, Ontario, Canada M5G 2C4.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: Two blinded reviewers separately assessed contrast-enhanced CT and nonenhanced and contrast-enhanced MR images in 30 patients with acute pancreatitis and established a severity index based on the presence of peripancreatic fluid collections and pancreatic necrosis. The Spearman rank correlation coefficient and weighted 
statistic were used to assess the correlation between each imaging technique and the interobserver agreement, respectively. Correlation between hospitalization days, morbidity, and severity indexes were assessed by using linear correlation.
RESULTS: A strong correlation existed for both reviewers when comparing contrast-enhanced CT with nonenhanced (r = 0.82, 0.79) or contrast-enhanced (r = 0.82, 0.79) MR cholangiopancreatography or when comparing nonenhanced and contrast-enhanced MR cholangiopancreatography (r = 0.99, 1.00). The interobserver agreement in staging was stronger with nonenhanced ( = 0.76) and contrast-enhanced ( = 0.78) MR cholangiopancreatography than with contrast-enhanced CT ( = 0.70). There was no linear correlation between the severity index for contrast-enhanced CT and outcome, while there was a linear correlation between nonenhanced or contrast-enhanced MR cholangiopancreatographic staging and the patient morbidity rate.
CONCLUSION: MR cholangiopancreatography could be an alternative to contrast-enhanced CT for the initial staging of acute pancreatitis.
Index terms: Pancreas, CT, 770.12113, 770.12115 • Pancreas, MR, 770.121411, 770.121412, 770.121415, 770.12143 • Pancreas, necrosis, 770.291 • Pancreatitis, 770.291, 770.3123, 770.45, 770.64
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Contrast medium–enhanced computed tomography (CT) is currently considered the standard of reference for diagnosing and staging acute pancreatitis (3), and its indications, as well as the CT nomenclature, have recently been reviewed (4,5). Contrast-enhanced CT allows the detection and grading of pancreatic necrosis and acute fluid collections, and these parameters have been shown to correlate with the course of the disease (6).
Recent reports (7–11) of both animal and human studies, however, have questioned the safety of injecting iodinated contrast medium during the early stage of acute pancreatitis. Magnetic resonance (MR) imaging, which until now has seldom been used in the setting of acute pancreatitis, may be an alternative to contrast-enhanced CT. Initial experimental data (12–14) have shown that MR cholangiopancreatography did not allow differentiation between edematous and hemorrhagic pancreatitis. However, three recent studies (15–17) have reported similar results between contrast-enhanced CT and MR cholangiopancreatography in diagnosing pancreatic necrosis and acute fluid collections.
The purpose of this study was (a) to evaluate the correlation between contrast-enhanced CT, nonenhanced MR cholangiopancreatographic, and contrast-enhanced MR cholangiopancreatographic findings in patients with acute pancreatitis, (b) to measure the interobserver agreement in staging acute pancreatitis with each technique, and (c) to correlate the results of these imaging techniques with patient outcome.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Thirty patients (17 men, 13 women) with a mean age of 52.3 years and an age range of 22–86 years were included in the study. The diagnosis of pancreatitis was based on the clinical manifestation and an elevation of the serum amylase level. The mean amylase level in the patient population was 2,226 U/L (range, 120–25,120 U/L), and the upper limit of the normal range is 115 U/L. All patients were initially admitted to an intensive care unit and treated with intravenous fluid administration, intensive monitoring, and supportive therapy.
The mean Ranson score (Table 1), recorded within the first 48 hours of the patient's admission, was 2.53, with an SD of 1.22 and a range of 0–5. The first imaging test was performed within 1 week of the onset of symptoms in 23 patients, 1–2 weeks after onset of symptoms in two patients, and more than 2 weeks after onset of symptoms in five patients. The mean interval between CT and MR cholangiopancreatography was 1.20 days (range, 0–3 days; SD, 0.88).
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The average CT examination was 30 minutes. Because CT is more readily available for nonurgent or semiurgent examinations than is MR cholangiopancreatography, CT was performed as the initial test and MR examinations were performed later. Although this could represent a bias in the data acquisition if one admits that contrast-enhanced CT could worsen acute pancreatitis, this has been demonstrated only in an animal model (7) in which contrast-enhanced CT was performed within 6 hours of the onset of acute pancreatitis, while in our series, CT was always performed more than 12 hours after the onset of pancreatitis. No parameters were monitored that could indicate the worsening of acute pancreatitis after the injection of contrast medium during CT.
MR Cholangiopancreatography
MR cholangiopancreatography was performed with a 1.5-T superconducting magnet (Signa 5.4; GE Medical Systems, Milwaukee, Wis) by using a phased-array torso multicoil. An antispasmodic agent (two separate intravenous injections of 20 mg of hyoscine butylbromide [Buscopan; Boehringer Ingelheim, Burlington, Ontario, Canada]) was used to decrease bowel peristalsis. Our MR cholangiopancreatographic protocol was as described in the following paragraphs.
1. Fat-suppressed fast spin-echo (SE) T2-weighted imaging was performed by using the following parameters: 4,000/112 (effective)(repetition time msec/effective echo time msec), echo train length of 16, section thickness of 7 mm with a 20% intersection gap, and a matrix size of 256 x 256.
2. Conventional SE T1-weighted imaging was performed with and without fat suppression. Conventional SE T1-weighted sections were acquired by using 400/10 (repetition time msec/echo time msec), a section thickness of 5 mm with a 20% intersection gap, and a matrix size of 256 x 192. The repetition time was increased to 500 msec for fat-suppressed conventional SE T1-weighted acquisitions.
3. In addition, a series of fast spoiled gradient-echo contiguous 7-mm-thick axial sections were obtained by using 120/4.2, a flip angle of 70°, and a matrix size of 256 x 128 prior to and immediately following the intravenous administration of gadopentetate dimeglumine (Magnevist; Berlex, Wayne, NJ; 0.1 mmol/kg body weight).
4. Finally, a delayed fat-suppressed conventional SE T1-weighted sequence (500/10) was performed. The fast SE T2-weighted sequence was used to cover the entire abdomen from the diaphragm to the iliac crests, while the conventional SE T1-weighted sequences and the gradient-echo sequence were limited to the pancreas and were used to cover the entire pancreatic bed. MR examinations lasted about 60 minutes.
Image Analysis
Contrast-enhanced CT images and nonenhanced and contrast-enhanced MR images were analyzed separately and independently by two experienced abdominal imagers (P.M.B., C.R.) who were blinded to the diagnosis and the patient's identity.
The reviewers (P.M.B., C.R.) have extensive experience in interpreting both CT and MR studies of the pancreas. The reviewers were presented with hard-copy images printed by using a commercial laser camera and a 12-image-per-page display. The degree of pancreatic necrosis and the presence and extension of acute peripancreatic fluid collections were scored according to the severity index developed by Balthazar et al (6). The same scoring system was used for contrast-enhanced CT, nonenhanced MR cholangiopancreatography, and contrast-enhanced MR cholangiopancreatography.
Contrast-enhanced CT
Both nonenhanced and contrast-enhanced CT images were made available to the reviewers. The severity of the acute inflammatory process, on the basis of the presence and extension of acute peripancreatic fluid collections, was divided into five categories: grade A (score = 0), normal pancreas; grade B (score = 1), focal or diffuse pancreatic enlargement (including contour irregularities, heterogeneous attenuation of the gland, dilatation of the pancreatic duct, and small foci of fluid collections within the gland with no peripancreatic disease); grade C (score = 2), intrinsic pancreatic abnormalities with haziness and streaky opacities representing inflammatory changes in the peripancreatic fat; grade D (score = 3), single, ill-defined fluid collection (low-attenuation, poorly defined fluid collections with no recognizable capsule or wall); and grade E (score = 4), two or more poorly defined fluid collections or the presence of gas in or adjacent to the pancreas. The presence and extent of pancreatic necrosis were also recorded. Necrosis was defined as a focal or diffuse, well-marginated area of nonenhancing pancreatic parenchyma. Enhancement was estimated semiquantitatively by comparing pancreatic attenuation with splenic attenuation at the hepatic portal venous phase. Present necrosis was described as that involving less than 33% of the volume of the pancreas (severity index score = 2) or less than 50% (score = 4) or more than 50% (score = 6) of the pancreatic tissue.
Nonenhanced MR Cholangiopancreatography
The pancreas was classified as normal (grade A) when it was of homogeneous signal intensity and hyperintense relative to liver on images obtained with fat-suppressed short repetition time sequences (15,18). Grade B was defined as heterogeneous signal intensity without peripancreatic fat involvement. Grade C was defined by the presence of stranding within the peripancreatic fat (15). Grades D and E were defined as one (grade D) or several (grade E) acute fluid collections seen as confluent and ill-defined peripancreatic areas of homogeneous or heterogeneous signal intensity but without a wall or capsule. Gas (grade E) was defined as an area of low signal intensity on images obtained with short and long repetition times and was associated with a magnetic susceptibility artifact. Necrosis was diagnosed when well-marginated areas of signal intensity different from the signal intensity of the normal pancreas were present (19).
Contrast-enhanced MR Cholangiopancreatography
Reviewers were provided with both nonenhanced and contrast-enhanced MR images. In addition to the parameters described in the preceding paragraphs, the reviewers were asked to record the degree of enhancement of inflammatory lesions and perform a semiquantitative evaluation of pancreatic enhancement on the postcontrast MR images.
At the end of each review, the severity index was calculated by adding the scores for acute inflammatory changes and pancreatic necrosis.
Statistical Analysis
Correlation between the CT and MR examinations.—The nonparametric Spearman rank test was used to assess the correlation between contrast-enhanced CT, nonenhanced MR cholangiopancreatography, and contrast-enhanced MR cholangiopancreatography for each reader scoring acute pancreatitis. The 95% CI for r and the two-tailed P value in testing the null hypothesis were also calculated. A P value less than .05 was considered as significant.
Interobserver agreement.—The weighted statistic (20) was used to measure the degree of agreement between the two observers in staging acute pancreatitis at contrast-enhanced CT, nonenhanced MR cholangiopancreatography, and contrast-enhanced MR cholangiopancreatography. In the calculation of the values, the four scores of pancreatic inflammation and the four scores of pancreatic necrosis were taken into account, while the scores of the severity index were divided into five categories: 0–2, 3–4, 5–6, 7–8, and 9–10. The weight of the values was calculated as follows: Concordant results were weighted 1.00. Discordant results in evaluating pancreatic inflammation or index of severity were weighted 0.75, 0.50, 0.25, and 0, depending on the degree of discordance. Discordant results in evaluating pancreatic necrosis were weighted 0.66, 0.33, and 0, depending on the degree of discordance. A weighted statistic of 0.41–0.60 was considered to indicate moderate agreement, a weighted statistic of 0.61–0.80 was considered to indicate good agreement, and a weighted statistic of 0.81–1.00 was considered to indicate excellent agreement (21).
Correlation with Patient Outcome
The following variables were considered in the outcome measures: days of hospitalization; rate of morbidity, defined as the presence of pancreatic sepsis (confirmed with needle aspiration or surgery), a well-defined pseudocyst, or the need for pancreatic surgery during the course of the disease (excluding delayed laparoscopic cholecystectomy); and rate of mortality.
The correlation between the Ranson criteria (Table 1), the severity index calculated by using contrast-enhanced CT images, nonenhanced MR images, and contrast-enhanced MR images, and these variables was assessed by using linear correlation. For this purpose, the scores of the two observers were averaged according to the technique described by Obuchowski and Zepp (22). We classified the severity indexes on a three-point scale (scale of 0–3, 4–6, and 7–10) similar to the one used by Balthazar et al (6) for comparison.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Correlation between CT and MR Findings
There was a significant correlation for both observers between the results of contrast-enhanced CT and nonenhanced MR cholangiopancreatography (Table 2). The correlation was not modified when the results of contrast-enhanced MR cholangiopancreatography were taken into consideration. In fact, there was an almost perfect correlation between nonenhanced and contrast-enhanced MR cholangiopancreatography in the calculation of the severity index and in the evaluation of the inflammatory process and pancreatic necrosis.
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statistic of 0.61–0.80). Overall, the interobserver agreement was stronger with MR cholangiopancreatography than with contrast-enhanced CT. In the evaluation of contrast-enhanced CT images, was 0.70, 0.62, and 0.71 for the severity index, inflammatory process, and pancreatic necrosis, respectively. In the evaluation of nonenhanced MR images, was 0.76, 0.72, and 0.78 for the severity index, inflammatory process, and pancreatic necrosis, respectively. In the evaluation of contrast-enhanced MR images, was 0.78, 0.74, and 0.78 for the severity index, inflammatory process, and pancreatic necrosis, respectively. With contrast-enhanced CT, the main interobserver discrepancy occurred between grades C and D (three [10%] of 30 patients) and D and E (five [17%] of 30 patients). Also, there was disagreement about the presence of necrosis in four patients (13%). For both nonenhanced and contrast-enhanced MR images, the main interobserver discrepancy occurred between grades D and E (three [10%] of 30 patients) or for identifying the presence of necrosis in three (10%) of 30 patients.
Correlation of the Results of CT and MR Cholangiopancreatography with Patient Outcome
The mean length of hospitalization was 39.10 days (range, 1–135 days; SD, 36.45). Complications occurred in 16 (53%) of the 30 patients. Sepsis was observed in 13 patients (43%) and was proved by means of fine-needle aspiration biopsy in five patients and by means of surgery in the remaining eight patients. Pancreatic pseudocysts developed in 13 (43%) of the 30 patients. Four patients were treated solely with percutaneous drainage, seven patients underwent percutaneous drainage followed by surgery, and the remaining two patients were treated conservatively.
Overall, nine (30%) of the 30 patients underwent surgery; indications for surgery included infected pseudocyst (n = 7), pancreatic abscess secondary to pancreatic necrosis (n = 1), and duodenal stenosis (n = 1). Six patients underwent delayed elective laparoscopic cholecystectomy; these patients were not included in the morbidity count.
Two (6%) of the 30 patients with postoperative pancreatitis died after at least one other surgery. Two additional patients died of unrelated causes at 6 and 8 months after resolution of their pancreatitis, and these deaths were not included in the mortality count.
There was a strong linear correlation between the measured Ranson score and the outcome parameters (Table 3). The morbidity rates for alcoholic, postoperative, drug-related, and gallstone pancreatitis were 100% (four of four patients), 80% (four of five patients), 60% (three of five patients), and 36% (four of 11 patients), respectively. The morbidity rate was 20% (n = 1) in the remaining five patients with pancreatitis.
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The administration of contrast material is mandatory for the evaluation of pancreatic necrosis, since diagnosis of necrosis is based on the lack of enhancement of pancreatic tissue. It is recommended that large volumes of contrast material be used and that the pancreas be imaged at the time of peak pancreatic arterial perfusion to improve the detection of pancreatic necrosis and peripancreatic inflammatory changes (23). However, recent experimental data (10,11) have shown that intravenous administration of contrast material could increase the number of cases of pancreatic necrosis in animals with experimentally induced acute pancreatitis. This may be related to impaired pancreatic perfusion, which results in trypsinogen activation and increased pancreatic necrosis (8). Some authors (24) have claimed that routine use of intravenous contrast material in the assessment of acute pancreatitis may not be necessary.
Although the issue remains controversial, the intravenous administration of iodinated contrast material could have a deleterious effect in patients with acute pancreatitis (25). In addition, contrast medium injection may further impair renal function in patients with acute pancreatitis. These potential risks related to the use of iodinated contrast material in patients with acute pancreatitis have prompted us to evaluate the use of MR cholangiopancreatography in this setting.
The first objective of this study was to compare MR and CT findings of acute pancreatitis. MR cholangiopancreatography currently plays a minor role in the routine work-up in patients with pancreatic diseases. However, recent technical advances, including phased-array multicoils, fat suppression, and gradient moment nulling, allow acquisition of images with excellent contrast resolution between pancreatic tissue and surrounding organs and/or lesions with an acceptable spatial resolution (18).
Published articles (16,17) have shown that MR cholangiopancreatography is a promising tool in the setting of acute pancreatitis, but these data remain limited. These articles reported that T2-weighted and gadolinium-enhanced T1-weighted sequences were useful in assessing severe pancreatitis and proposed criteria to grade inflammatory changes and necrosis with MR cholangiopancreatography instead of CT.
In these studies, however, correlations between CT and MR data are questionable because the time between the examinations was too long. In our study, 30 patients were included, and all patients underwent CT and MR examinations over less than 3 days; therefore, we believe that our results of comparing CT and MR cholangiopancreatography are likely to be more accurate. We found a good correlation between CT and MR cholangiopancreatography in the evaluation of both fluid collections and pancreatic necrosis. Acute fluid collections were mainly hypoattenuating on CT images but appeared more heterogeneous on MR images. Ward et al (17) attributed the signal intensity characteristics to hemorrhage because acute fluid collections appeared hyperintense on both T1- and T2-weighted images. In our series, the signal intensity of these acute fluid collections was more complex. They primarily were hyperintense on fat-suppressed T1-weighted images and contained areas of high and low signal intensity on T2-weighted images (Fig 1).
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values for CT, nonenhanced MR cholangiopancreatography, and contrast-enhanced MR cholangiopancreatography indicated good interobserver agreement for the three imaging studies. For CT and MR cholangiopancreatography, the agreement was better in assessing necrosis than in staging the severity of the inflammatory process. For necrosis, disagreement was observed in patients with tiny, nonenhancing lesions within the pancreas, which were diagnosed as foci of edema by one observer and as tiny foci of necrosis by the other observer. In our opinion, this result highlights the difficulties in classifying these entities. Surgical correlation proved that small areas of patchy pancreatic necrosis may not be detected at contrast-enhanced CT (27). Moreover, it has been shown that most small, nonenhancing lesions within the pancreas disappear by the time of follow-up CT, indicating that they were due to edema (28). Because the CT findings of necrosis may be equivocal at the onset of pancreatitis, it has been recommended that the initial CT scanning be postponed (29,30). For MR cholangiopancreatography, results of an experimental study (12) have suggested that the relaxation time of necrosis increases over time. This finding could be helpful in differentiating nonenhancing edema from necrosis; however, results from our study cannot confirm this hypothesis because follow-up MR examinations were not included in our protocol.
In staging the severity of the inflammatory process, a discrepancy was observed for eight (27%) of 30 patients on contrast-enhanced CT images and for three (10%) of 30 patients on both nonenhanced and contrast-enhanced MR images. This superiority of MR cholangiopancreatography over contrast-enhanced CT may be related to the ability to accurately detect and characterize hemorrhagic-like peripancreatic collections and separate them from inflammatory changes without fluid at MR cholangiopancreatography. Fat suppression facilitated the detection of hyperintense hemorrhagic-like peripancreatic collections against a background of hypointense saturated peripancreatic fat (Fig 4).
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We classified the severity index on a three-point scale similar to the one used by Balthazar et al (6). We did not find any correlation between the three-point-scale severity index and the length of hospitalization. However, we believe that length of hospitalization may not provide an accurate representation of morbidity, since social factors or elective surgery may prolong the length of stay. The number of fasting days could be a more objective parameter; unfortunately, this information was not included in the design of our study and was not available retrospectively from the patient charts.
We did not find a progressive increase in the morbidity rate in the three groups of patients differentiated according to the CT severity index. However, patients with a CT severity index of 0–3 had a markedly lower morbidity rate than did patients with higher indexes. Our results are in disagreement with those reported by Balthazar et al (6), who showed that the morbidity rate in patients with pancreatitis increased continuously with the degree of necrosis graded at CT and with the severity index. However, the prognostic value of CT grading remains controversial, since London et al (31) did not report any correlation between the site and extent of necrosis and pancreatitis severity.
Our results showed a progressive increase in the morbidity rate in the three groups of patients when we used the MR cholangiopancreatographic index of severity. We cannot definitively conclude that MR cholangiopancreatography is superior to CT in the evaluation of the prognosis in patients with acute pancreatitis because of the small number of patients included in our study; further evaluation of a larger number of patients is required to confirm this hypothesis. Also, the unique ability of MR cholangiopancreatography to depict abnormalities such as hemorrhagic-like collections and its superior characterization of pseudocysts (17) could broaden the applications and increase the usefulness of MR cholangiopancreatography in evaluating prognosis and predicting outcome in patients with acute pancreatitis.
The limitations of our study include the small number of patients studied, the delay between the onset of symptoms and the imaging examinations, and the absence of correlation between imaging and macroscopic data. Another limitation is that there is no standard of reference for determining which criteria should be used to evaluate the severity of acute pancreatitis with imaging.
Unlike in other studies (6), in our study we preferred to use the time between the onset of symptoms and the imaging examinations in our calculations rather than the time between admission and the imaging examinations, since the former interval begins with the symptomatic onset of pancreatitis. In our study, most patients underwent imaging within the 1st week of the symptoms; only a few patients underwent imaging more than 1 week after the onset of symptoms, and, in those patients, evaluation of the severity index on CT or MR images may not have provided prognostic information as accurate as the information that would have been obtained from an examination performed sooner after the onset of symptoms.
The absence of correlation between imaging and macroscopic data is a major limitation of our study. Even for patients who underwent surgery, correlations are not reliable because of the long time between imaging and surgery. Correlation with surgical and pathologic data is mandatory to establish the value of imaging in diagnosing small areas of intrapancreatic necrosis or in distinguishing peripancreatic inflammation from peripancreatic collections. However, patients with such imaging findings generally do not require surgery. Thus, experimental studies will be helpful to correlate imaging and pathologic data.
In conclusion, nonenhanced MR cholangiopancreatography is a reproducible method for staging acute pancreatitis and is at least as accurate as CT in establishing the prognosis of disease. It should be preferred to CT in patients with renal failure. If further evaluation does confirm that intravenous administration of iodinated contrast material may lead to an increase in the number of cases of pancreatic necrosis, MR cholangiopancreatography could become the main imaging modality for patients with acute pancreatitis. Moreover, the addition of a heavily T2-weighted sequence, or an MR cholangiopancreatographic sequence, would increase the diagnostic range of the examination by allowing accurate detection of choledocholithiasis (17,32), which is one of the main etiologic factors of acute pancreatitis, along with alcohol abuse and pancreas divisum (33). This added information could have a substantial effect on the management of acute pancreatitis. However, to date, to our knowledge, the accuracy of MR cholangiopancreatography in the detection of either choledocholithiasis or pancreas divisum in the presence of severe acute pancreatitis has not been established. Also, because of its cost and its inability to be used to guide interventional procedures, MR cholangiopancreatography's role in the staging and management of pancreatitis has to be confirmed with larger studies, including cost-effectiveness analysis.
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Footnotes |
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Author contributions: Guarantors of integrity of entire study, R.L., P.M.B.; study concepts, P.M.B., C.R.; study design, P.T., P.M.B., C.R.; definition of intellectual content, P.M.B., P.T.; literature research, P.T., R.L.; clinical studies, P.M.B., C.R., M.A.; data acquisition, P.M.B., C.R., M.A.; data analysis, P.T., R.L.; manuscript preparation, R.L., P.M.B., P.T.; manuscript editing and review, P.M.B., P.T., R.L., M.A.
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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