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(Radiology. 2001;218:61-67.)
© RSNA, 2001

Gastrointestinal Imaging

MR Hydrometry to Assess Exocrine Function of the Pancreas: Initial Results of Noninvasive Quantification of Secretion1

Johannes T. Heverhagen, MSc, Daniela Müller, MD, Anke Battmann, MD, Natascha Ishaque, MD, Dominik Boehm, MSc, Martin Katschinski, MD, PhD, Hans-Joachim Wagner, MD, PhD and Klaus J. Klose, MD, PhD

1 From the Departments of Diagnostic Radiology (J.T.H., A.B., N.I., H.J.W., K.J.K.) and Gastroenterology (D.M., M.K.), PU Marburg, University Hospital, Philipps University, Baldingerstrasse, 35033 Marburg, Germany; and the Center for Medical Diagnostic Systems and Visualization GmbH, University of Bremen, Germany (D.B.). Received March 3, 2000; revision requested April 25; revision received May 26; accepted June 28. Address correspondence to J.T.H. (e-mail: heverhag@post.med.uni-marburg.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate magnetic resonance (MR) hydrometry, a method of quantifying fluid amounts by using MR imaging, for assessing the exocrine function of the pancreas after stimulation with secretin.

MATERIALS AND METHODS: Images were obtained with a single-shot turbo spin-echo sequence by using a 1.0-T magnet with a quadrature body coil. Image postprocessing and evaluation were performed at an external workstation by using a specially designed histogram algorithm that translates the MR signal intensity of duodenal filling into an actual amount of duodenal fluid. This algorithm was tested in vitro and in vivo. Finally, MR hydrometry results in five patients were correlated with those of the secretin-cerulein test.

RESULTS: The phantom measurements showed a high correlation (r = 0.99) between the actual amount of fluid in the imaging volume and the calculated results. In vivo, the ability of MR hydrometry to enable exact quantification of fluid amounts was demonstrated. In correlating the signal intensity of duodenal filling with the exact amount of additional fluid in the duodenum in volunteers, a coefficient of 0.043 gray tones per pixel per milliliter was calculated. The correlation (r) between secretin-stimulated duodenal fluid output estimated by using tube aspiration and that estimated by using MR hydrometry was 0.946 (P < .05).

CONCLUSION: MR hydrometry is a promising noninvasive method of assessing fluid output as a measure of exocrine pancreatic function.

Index terms: Magnetic resonance (MR), cholangiopancreatography, 78.121411, 78.121416, 78.12144 • Magnetic resonance (MR), comparative studies, 78.121411, 78.121416, 78.12144 • Magnetic resonance (MR), experimental studies, 78.121411, 78.121416, 78.12144 • Magnetic resonance (MR), volume measurement, 78.12144 • Pancreas, function, 770.91 • Pancreas, MR, 770.121411, 770.121416, 770.12144 • Secretin


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Advances in magnetic resonance (MR) techniques have enabled authors such as Soto et al (1) and Guibaud et al (2) to visualize the morphology of the hepatobiliary system and pancreatic ducts in healthy volunteers and patients with pathologic conditions of the liver or pancreas. The use of secretin improves the visibility of pancreatic ducts by stimulating the exocrine function of the gland (3,4) and thus improves the certainty of morphologic diagnoses.

The reference standards for examining the exocrine function of the pancreas are tube examinations; the effectiveness of the secretin-cerulein test has been extensively validated (5,6). To perform this examination, intubation of the gastrointestinal tract, which causes patient discomfort, is mandatory. In addition, the procedure and its evaluation are time-consuming, expensive, and can be performed in only a few highly specialized laboratories. Compared with endoscopic retrograde cholangiopancreatography, which is used to assess morphologic changes in patients with chronic pancreatitis, the secretin-cerulein test has higher accuracy in the diagnosis of chronic pancreatitis (5). Moreover, the morphologic appearance of the pancreatic ducts may be influenced by various pathologic conditions—for example, scars due to acute or chronic pancreatitis, and atrophy in elderly subjects.

Realizing the importance of testing exocrine function to diagnose chronic pancreatitis, especially that in the early stages, many groups are searching for noninvasive examinations with results that reveal early-stage pancreatic dysfunction. Analysis of chymotrypsin concentration in feces does not appear to be sufficient (7). The fecal elastase test is an improvement. Elastase is not degraded in transit along the gastrointestinal tract, but rather it is concentrated in feces. Fecal elastase has been shown to be a reliable parameter for detection of advanced stages of chronic pancreatitis (7–11). However, in at least three of studies (5,10,11), fecal elastase was shown to be insensitive in recognizing early-stage chronic pancreatitis with only slight functional disturbances.

Another noninvasive examination is the fluorescein dilaurate test. This test enables one to quantify the potency of pancreas-specific cholesterolesterhydrolase to split fluorescein dilaurate. However, according to the Cambridge classification (12), this test has a sensitivity of only 50% in the diagnosis of stages I and II chronic pancreatitis.

Recently available procedures to measure the exocrine secretion of the pancreas are breath tests that involve stable radioisotopes. Two examples are the carbon 13 Hiolein breath test and the cholesteryl-octanoate breath test with 13C or carbon 14 (13). Although both of these tests are used to diagnose pancreatic steatorrhea, they cannot enable the detection of early-stage chronic pancreatitis with moderately reduced enzyme secretion.

An alternative approach to hormonal stimulation of the pancreas is based entirely on secretin-induced fluid and bicarbonate secretion (14). An approach to measuring secretion at MR imaging was proposed by Matos et al (15). These authors developed a system of estimating the filling of the duodenum on the basis of pancreatic secretion after secretin stimulation. This attempt provided an early hint at the capability of secretin-stimulated MR hydrometry to replace invasive intubation procedures. The purpose of our study was to assess the exocrine function of the pancreas after secretin stimulation by using a specially developed MR imaging algorithm.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
All investigations were performed by using a 1.0-T clinical magnet (Magnetom Expert; Siemens, Erlangen, Germany), commercially available gradients capable of a 1,200-µsec rise time and 20 mT/m maximum gradient strength, and a quadrature body coil. To depict all fluid in the imaging volume, we chose a fluid-sensitive spin-echo MR sequence. We used a dynamic breath-hold single-shot turbo spin-echo T2-weighted sequence ({infty}/1,100 [repetition time msec/echo time msec], 150° refocusing pulse flip angle) with an acquisition time of 7 seconds. The echo train consisted of 240 echoes. We acquired single sections with an in-plane resolution of 1.00 x 0.94 mm and a voxel depth of 65 mm. This provided a summation of all fluids in the imaging volume. Measurements were repeated at different time points (every 30 seconds up to 10 minutes). Quantitative evaluation of the obtained images was performed with a specially designed histogram algorithm (IMAGELAB; MeVis, Bremen, Germany) to calculate the absolute amount of fluid increase. This software was run on an Indigo2 workstation (Silicon Graphics, Mountain View, Calif). The quantity of fluid in the imaging volume in a given time interval, QF(t), was calculated according to the equation QF(t) = [{Sigma}I I x NI(t)]/N, where I is the pixel signal intensity; NI, the number of pixels with I; {Sigma}I, the sum of all I values; and N, the total number of pixels.

The difference in the quantity of fluid between each time point (t > 0 seconds) and the starting volume (t = 0 seconds) was determined by using the equation {Delta}QF(t) = QF(t) - QF(t = 0), where {Delta}QF(t) is the calculated change in fluid quantity in the imaging volume in a given time interval.

In Vitro Experiments
Theoretic considerations pointed to potential problems concerning the measurements and their evaluation. Problems could occur owing to (a) the nonreproducibility of signal intensity with repeated measurements, (b) a possible nonlinearity in signal intensity increase parallel to an increasing fluid volume, (c) a saturation of visualized fluid due to former excitations, and (d) the confounding influence of volume thickness and pixel size.

The following model was used for the in vitro examinations: To demonstrate the reproducibility of our measurements, we used a power injector (Spectris; MedRad, Maastricht, the Netherlands) to steadily fill a reservoir with water. The other studies were performed by using a phantom that consisted of ultrasonographic gel, fat, and a reservoir for water. The phantom also was filled with the power injector.

Signal intensity reproducibility was evaluated by acquiring the same section 20 times, with a delay of about 2 minutes between each measurement. Mean values and coefficients of variation (SD divided by mean value) were calculated. To show the linear correlation between additional fluid in the imaging volume and calculated change in fluid quantity in the imaging volume, {Delta}QF, an increasing amount of saline solution (0–30.0 mL in 0.25-mL increments; 30–120 mL in 10-mL increments) was measured. The factor c for correlating the surplus of fluid V with {Delta}QF was calculated by using the equation c = {Delta}QF/V.

The time course of the saturating effect was measured by processing sets of two images. The first image was acquired to presaturate the imaging volume; and the second image, to assess the saturation effect. The delays between the first and second image acquisitions were increased stepwise from 7 (immediately after the end of the first measurement) to 30 seconds. The delay between each set of measurements was 1 minute.

The influence of volume thickness was quantified by measuring a 65-mm-thick phantom that contained increasing amounts of fluid (0–150 mL). Different imaging volumes (40–150 mm in 10-mm increments) were acquired. For each volume, the gradient of the relation of {Delta}QF to actual amount of fluid in the volume was calculated. Therefore, whether a change in the gradient correlated with volume thickness only or also correlated with the tissue covered in the imaging section could be determined. The same experiment was performed with varying pixel sizes (0.83 x 0.78 mm to 2.08 x 1.95 mm).

Animal Model
A transnasal tube was advanced, with fluoroscopic guidance, into the duodenal lumen of an anesthetized pig (50 kg). The pig was positioned in the MR imaging unit. Saline solution (100 mL) was administered in 5-mL increments. This animal experiment was approved by the animal care and animal experimental commission of the government of the state of Hessia, Germany.

Volunteers
Ten volunteers (six male, four female; mean age [± SEM], 23.4 years ± 1.9; age range, 23–44 years) with no known intestinal disorders were intubated with a duodenal probe and examined while in the MR imaging unit. Saline solution (95 mL) was instilled in 5-mL increments during the investigation. Before starting each measurement, an aliquot of 5 mL was instilled. The {Delta}QF values were compared with the actual increases in volume. This correlation yielded c for translation of the incremental signal intensity of duodenal filling into an actual volume increase. The group mean and SD of c were then calculated. This portion of the study was approved by the institutional review board of the University Hospital of Philipps University, and written informed consent was obtained from all volunteers.

Patients
The {Delta}QF values in five patients (one woman, four men; mean age, 52.8 years ± 5.3; age range, 33–66 years) who routinely underwent a secretin-cerulein test and were referred for MR cholangiopancreatography were correlated with the results of their secretin-stimulated MR examinations. The fluid volumes after secretin stimulation estimated by using tube aspiration and MR hydrometry were correlated. The study involving patients was approved by the same institutional review board, and written informed consent was obtained from all subjects.

Statistical Analysis
All calculations and statistical tests were performed by using statistical software (SPSS, Chicago, Ill) based on a standard personal computer system. To compare the MR hydrometry and tube test results, we used the Pearson correlation coefficient. A P value of less than .05 was considered to indicate statistical significance. Values were displayed with the SEM unless otherwise stated.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In Vitro Experiments
The reproducibility measurements revealed a coefficient of variation of 0.18% (Fig 1). Furthermore, the measurements showed a linear correlation between the actual amount of fluid in the imaging volume and the {Delta}QF. The gradient of the regression line in Figure 2 is 0.027 gray tones per pixel per milliliter of fluid, and the regression coefficient (R2) is 0.99.



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  		Figure 1. Box plots of repeated measurements (n = 20) of a known fluid volume (90 mL), with a delay of 2 minutes between each measurement. The mean value obtained from these 20 experiments was 27.4 gray tones per pixel, with a low coefficient of variation, 0.18%. Original data are presented in the left box plot; in the box plot on the right, median values (horizontal lines), quartile values (box), and the range of values (vertical line) are illustrated. QF = quantity of fluid.

 


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  		Figure 2. Linear correlation between the {Delta}QF and the actual increase in fluid in the imaging volume reveals a gradient of the regression line of 0.027 gray tones per pixel per milliliter of fluid. A scattergram of the differences in gray tones per pixel for defined increasing fluid volumes is shown. The volume increased from 0 to 30 mL in 0.25-mL increments and from 30 to 120 mL in 10-mL increments.

 
The correlation of the {Delta}QF on the presaturated images with the delay between the presaturation and imaging sequences is demonstrated in Figure 3. The strong presaturation effect of short delays up to 6 seconds was clearly recognizable. A delay of 6–11 seconds led to only a slight presaturation effect, and delays longer than 11 seconds had no presaturation effects. Neither pixel size nor volume thickness influenced the correlation between {Delta}QF and actual quantity of fluid in the imaging volume.



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  		Figure 3. Graph illustrates the results of repeated single-shot turbo spin-echo MR imaging of the same defined fluid volume (150 mL), with an increasing delay between every two measurements. The saturation effect according to the delay between a presaturating sequence and a saturated measurement are shown. Delays shorter than 6 seconds led to a strong saturation effect of the preceding turbo spin-echo sequence. Delays of 6-11 seconds created only a slight saturation effect, and longer delays had no influence of the presaturation measurement.

 
Volunteers
The graph in Figure 4 illustrates the {Delta}QF in a volunteer during the investigation. The mean {Delta}QF in the 10 volunteers was 4.1 gray tones per pixel ± 0.22 at the end of the investigation. The data on all the volunteers are summarized in Table 1, and the regression lines correlating the {Delta}QF with the actual administered volume (95 mL) are displayed in Figure 5a. From the correlation of {Delta}QF and actual administered volume (95 mL) in vivo, the coefficient for derivation of the actual volume from the {Delta}QF was calculated. For in vitro testing, the gradient was 0.027 gray tones per pixel per milliliter (Fig 2), whereas in vivo imaging revealed a gradient of 0.043 gray tones per pixel per milliliter. Figure 5b shows a box plot of the derived coefficients. For example, an increase in {Delta}QF of 4.085 gray tones per pixel gives an increase in fluid volume of 95 mL.



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  		Figure 4. Evaluation of fluid increases measured with MR hydrometry compared with the actual instilled volumes (5 mL per measurement step) in a healthy volunteer. The linear regression graph shows a steady increase in measured fluid in the imaging volume with every 5-mL increment of instilled fluid.

 

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  		TABLE 1. Differences in Fluid Quantity with Instillation of 95 mL of Saline Solution in 10 Volunteers
 


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  		Figure 5a. (a) Graph of linear regression lines of increasing {Delta}QF in all 10 healthy volunteers. (b) Box plot of the regression line gradients demonstrates low variation. The horizontal lines denote median values; the box, quartile values; and the vertical line, the range of values.

 


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  		Figure 5b. (a) Graph of linear regression lines of increasing {Delta}QF in all 10 healthy volunteers. (b) Box plot of the regression line gradients demonstrates low variation. The horizontal lines denote median values; the box, quartile values; and the vertical line, the range of values.

 
Patients
The native image (Fig 6a) and the images obtained after secretin stimulation (5.0 [Fig 6b], 8.0 [Fig 6c], and 9.5 minutes [Fig 6d]) after stimulation) in patient 4 are shown in Figure 6. Even qualitative morphologic analysis of the four images clearly demonstrated a substantial increase in fluid quantity in the duodenum and jejunum. The results of hydrometric analysis of MR cholangiopancreatography images obtained after secretin stimulation in patient 4 are shown in Figure 7. The increase in duodenal fluid collection started 1 minute after stimulation (as illustrated by the cutting point of the regression line with the x axis) and then continued to rise during the remaining imaging time. The MR hydrometry and test tube results in the patients are listed in Table 2, and the correlations of the fluid quantities measured at MR hydrometry with those derived from the tube test are illustrated in Figure 8. The calculation of the total increase in fluid quantity due to secretin stimulation revealed a secretion of 225.35 mL within the first 10 minutes. With the assumption of linear extrapolation, the fluid quantity per hour would be 1352.2 mL.



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  		Figure 6a. MR cholangiopancreatography images ({infty}/1,100) obtained in a 28-year-old man with suspected reduced exocrine pancreatic function (a) before stimulation with secretin and (b) 5.0, (c) 8.0, and (d) 9.5 minutes after secretin stimulation. (a-d) After secretin stimulation, the main pancreatic duct (arrows) is consistently better visualized. A continuously increasing filling of the duodenum (arrowheads in c and d) and jejunum (*) with fluid can be seen. This fluid increase was quantified with use of the described specially developed algorithm, an example of which is shown in Fig 7.

 


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  		Figure 6b. MR cholangiopancreatography images ({infty}/1,100) obtained in a 28-year-old man with suspected reduced exocrine pancreatic function (a) before stimulation with secretin and (b) 5.0, (c) 8.0, and (d) 9.5 minutes after secretin stimulation. (a-d) After secretin stimulation, the main pancreatic duct (arrows) is consistently better visualized. A continuously increasing filling of the duodenum (arrowheads in c and d) and jejunum (*) with fluid can be seen. This fluid increase was quantified with use of the described specially developed algorithm, an example of which is shown in Fig 7.

 


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  		Figure 6c. MR cholangiopancreatography images ({infty}/1,100) obtained in a 28-year-old man with suspected reduced exocrine pancreatic function (a) before stimulation with secretin and (b) 5.0, (c) 8.0, and (d) 9.5 minutes after secretin stimulation. (a-d) After secretin stimulation, the main pancreatic duct (arrows) is consistently better visualized. A continuously increasing filling of the duodenum (arrowheads in c and d) and jejunum (*) with fluid can be seen. This fluid increase was quantified with use of the described specially developed algorithm, an example of which is shown in Fig 7.

 


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  		Figure 6d. MR cholangiopancreatography images ({infty}/1,100) obtained in a 28-year-old man with suspected reduced exocrine pancreatic function (a) before stimulation with secretin and (b) 5.0, (c) 8.0, and (d) 9.5 minutes after secretin stimulation. (a-d) After secretin stimulation, the main pancreatic duct (arrows) is consistently better visualized. A continuously increasing filling of the duodenum (arrowheads in c and d) and jejunum (*) with fluid can be seen. This fluid increase was quantified with use of the described specially developed algorithm, an example of which is shown in Fig 7.

 


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  		Figure 7. Graph illustrates measured {Delta}QF (-{blacksquare}-) in the patient in Figure 6, plotted during the entire imaging time. A calculated regression line that shows the mean fluid output of the pancreas (straight line) also is shown. The {Delta}QF regression line crosses the x axis at 1 minute, which indicates the time when secretion began. At 9.5 minutes after secretion, the {Delta}QF reaches 9.2 gray tones per pixel, which corresponds to a total incremental fluid output of 225.35 mL.

 

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  		TABLE 2. Results of MR Hydrometry and Probe Tube Test in Five Patients
 


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  		Figure 8. The calculated exocrine fluid outputs measured at MR hydrometry (MRH) in all five patients ({blacklozenge}) plotted against the collected volumes measured with the tube test. The higher volumes with the tube test are explained by the prolonged sampling time, 60 minutes, compared with the sampling time for MR hydrometry, 10 minutes. All values below 300 mL/hour define an insufficient exocrine secretion, as measured with the tube test.

 
A comparison of the results of pancreatic fluid secretion obtained by using the secretin-cerulein test with those obtained by using MR hydrometry revealed a significant correlation (r = 0.946; P < .05; Pearson correlation coefficient) in the patient group.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
REFERENCES
 
The in vitro experiment results demonstrated the ability to quantify fluid volumes by using the described single-shot turbo spin-echo sequence with a histogram algorithm—that is, quantitative MR hydrometry. In a defined imaging volume, the fluid quantity was constant, as shown by a coefficient of variation below 1%. The actual amount of fluid in the volume correlated linearly with the {Delta}QF, with a coefficient of 0.027 gray tones per pixel per milliliter of fluid. Saturation effects were negligible with delays longer than 11 seconds between each measurement. The {Delta}QF varied with different amounts of tissue covered in the imaging volume. Thus, section thickness and pixel size were relevant factors in obtaining appropriate measurements.

The volunteer investigation enabled us to adapt the correlation between {Delta}QF and actual volume changes to humans in vivo. This correlation varied from that determined in the in vitro examinations owing to the higher mass of the humans compared with that of the phantom in the magnetic field. The results showed that the use of noninvasive MR hydrometry in humans is feasible. Differences in magnetic field, magnetic field homogeneity, gradient systems, coil arrangements, and sequence design make it necessary to adjust the measurement in each MR imaging system to allow correct quantification.

These first experiences with five patients showed promising results. Secretin-stimulated MR cholangiopancreatography combined with histogram algorithm analysis—that is, MR hydrometry—seems to have the potential to enable quantification of the amount of fluid produced by the exocrine pancreas following secretin stimulation. To validate this finding, however, further studies with more patients have to be conducted.

The assumption of a constant secretion for 1 hour could lead to overestimation in the quantification of fluid secretion. Among the five patients, the distinction between insufficient secretion in one patient (No. 3, Table 2) and normal secretion in the other patients was easy. In patients with only a slight disturbance in pancreatic secretion this distinction could be more difficult. Therefore, studies with larger patient populations are essential for a more valid comparison of secretin-cerulein test and MR hydrometry results.

With MR hydrometry, it is not possible to evaluate enzyme secretion. Whether the assessment of fluid output per se enables accurate classification of pancreatic function remains to be elucidated. Tube tests that involve hormonal stimulation are based also on bicarbonate and/or enzyme concentrations in duodenal juice (16).

In general, it can be concluded that MR hydrometry has some restrictions. It does not allow one to quantify a steady volume of fluid; only changes in volume can be measured. The characteristics of different imaging units, coils, sequences, and measurement parameters (eg, repetition time, echo time, and flip angle) necessitate adjustment of c for calculation of the actual fluid increase in the measured volume. The adjustment for different imaging units from the same manufacturer and with the same specifications in particular may be an obstacle in the implementation of MR hydrometry as a standard procedure. The variations in c with different sequences and imaging parameters make it essential to recalculate c at every institution. However, this can be easily done if our protocol is used and an investigation with a cohort (about 10) of healthy volunteers is performed. Administering a known amount of fluid and calculating the {Delta}QF allow validation of a protocol for fluid measurements.

Hydrometry also has many advantages compared with the standard procedures used to determine the exocrine function of the pancreas. MR hydrometry is noninvasive and fast. Because MR hydrometry is noninvasive, it involves no additional stimuli to the stomach or intestine for the secretion of fluid, which can compromise the results of invasive examinations.

In conclusion, the results of this study demonstrate the technical feasibility of quantifying duodenal fluid output by using MR hydrometry. Further studies to investigate the role of this technique as a tool to assess exocrine pancreatic function are warranted.


   ACKNOWLEDGMENTS
 
We thank P. Zoefel, PhD, of the Computer Center, Department of Statistics, Philipps University, Marburg, Germany, for his support in the statistical evaluation of our study results.


   FOOTNOTES
 
Abbreviation: {Delta}QF = calculated change in fluid quantity in the imaging volume

Author contributions: Guarantors of integrity of entire study, H.J.W., J.T.H., K.J.K., M.K.; study concepts, H.J.W., J.T.H., M.K.; study design, J.T.H., M.K.; definition of intellectual content, H.J.W., J.T.H., K.J.K., M.K.; literature research, A.B., J.T.H.; clinical studies, D.M., J.T.H., M.K.; experimental studies, D.B., J.T.H., N.I.; data acquisition, A.B., D.M., J.T.H., N.I.; data analysis, D.B., J.T.H., N.I., M.K.; statistical analysis, H.J.W., J.T.H.; manuscript preparation, J.T.H.; manuscript editing, D.B., H.J.W., M.K.; manuscript review, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 

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  6. Bozkurt T, Braun U, Leferink S, Gilly G, Lux G. Comparison of pancreatic morphology and exocrine functional impairment in patients with chronic pancreatitis. Gut 1994; 35:1132-1136.[Abstract/Free Full Text]
  7. Katschinski M, Schirra J, Bross A, Goke B, Arnold R. Duodenal secretion and fecal excretion of pancreatic elastase-1 in healthy humans and patients with chronic pancreatitis. Pancreas 1997; 15:191-200.[Medline]
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  12. Dominguez-Munoz JE, Pieramico O, Buchler M, Malfertheiner P. Clinical utility of the serum pancreorauryl test in diagnosis and staging of chronic pancreatitis. Am J Gastroenterol 1993; 88:1237-1241.[Medline]
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J. T. Heverhagen, H.-J. Wagner, H. Ebel, A. L. Levine, K. J. Klose, and A. Hellinger
Pancreatic Transplants: Noninvasive Evaluation with Secretin-augmented MR Pancreatography and MR Perfusion Measurements--Preliminary Results
Radiology, October 1, 2004; 233(1): 273 - 280.
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W Schwizer, M Fox, and A Steingotter
Non-invasive investigation of gastrointestinal functions with magnetic resonance imaging: towards an "ideal" investigation of gastrointestinal function
Gut, June 1, 2003; 52(90004): iv34 - 39.
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S. S. Sonnad
Describing Data: Statistical and Graphical Methods
Radiology, December 1, 2002; 225(3): 622 - 628.
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C. Matos, O. Cappeliez, C. Winant, E. Coppens, J. Deviere, and T. Metens
MR Imaging of the Pancreas: A Pictorial Tour
RadioGraphics, January 1, 2002; 22(1): e2 - e2.
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