First published online July 5, 2006
British Journal of Radiology (2006) 79, 804-807
© 2006 British Institute of Radiology
doi: 10.1259/bjr/41916828
Duplex ultrasound of the superior mesenteric artery in chronic pancreatitis
M Hornum, MD
1
S Larsen, MD, PhD
1
O Olsen, MD, PhD
3 and
J F Pedersen, MD, PhD
2
Departments of 1Gastroenterology and 2Radiology, Glostrup Hospital, Copenhagen and3Department of Surgical Gastroenterology, Amager Hospital, University of Copenhagen, Copenhagen, Denmark
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Abstract
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Blood flow in the superior mesenteric artery (SMA) increases after a meal due to a vasoactive effect of the decomposed food. In exocrine pancreatic insufficiency, the digestion of food is compromised. We used duplex ultrasound to test the hypothesis that blood flow in the SMA after a meal increases less in patients with pancreatic insufficiency than in control persons. We studied 16 patients with chronic pancreatitis, eight of them with exocrine insufficiency, and eight healthy volunteers. The resistive index (RI) in the SMA was determined before and after a liquid meal. The RI reflects the downstream circulatory resistance, giving a precise description of mesenteric hyperaemia. Both groups of patients with chronic pancreatitis unexpectedly had lower fasting RI than controls, 0.818 and 0.815 vs 0.851, p = 0.028 and p = 0.0030, respectively. Postprandialy there was significantly less decrease in RI (less increase in flow) in patients with exocrine insufficiency than in controls, 0.055 vs 0.099, p = 0.0047. There was a significant trend for a less pronounced postprandial decrease in RI with more impaired pancreatic function (p = 0.0036). Our study thus demonstrates a reduced postprandial increase in SMA flow in patients with exocrine pancreatic insufficiency, and suggests an increased fasting SMA flow in chronic pancreatitis. Further studies are needed to evaluate the possible role of the test-meal-induced shift in RI in the SMA and of a lower-than-normal fasting RI in the diagnosis and monitoring of chronic pancreatitis.
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Introduction
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At ultrasound scanning combined with the pulsed Doppler technique we can non-invasively monitor alterations in blood flow velocity. Applied to the superior mesenteric artery (SMA), the method confirms that blood flow in this vessel increases in response to a meal [1–3]. The vasoactive components seem to be influenced by the digestive products of the diet, so that the effect of a meal on splanchnic blood flow may depend on the intraluminal digestion [1]. Patients with end stage chronic pancreatitis are characterized by maldigestion due to exocrine pancreatic insufficiency, but it is not known whether the reduced intraluminal food digestion is mirrored in the mesenteric blood flow. It was our hypothesis that these patients would show less postprandial increase in mesenteric blood flow than control persons, so that the postprandial shift in Doppler velocity pattern might be used in the diagnosis and monitoring of chronic pancreatitis.
In this study we examine the velocity pattern in the SMA before and after a liquid test meal in patients with chronic pancreatitis with and without preserved exocrine function, and in healthy controls.
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Methods and patients
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We studied 16 patients with chronic pancreatitis, eight with minimal or no exocrine pancreatic function and eight with reduced exocrine function, and eight healthy volunteers (Table 1
). The aetiology of chronic pancreatitis was alcohol in 14 patients and unknown in two. All patients had moderate or marked imaging findings according to the Cambridge classification [4] plus reduced exocrine pancreatic function judged from the intraduodenal meal-stimulated lipase concentration (Lundh test), or steatorrhoea. The eight patients with exocrine insufficiency were characterized by a Lundh test result below 10% of the normal lower limit [5], or excretion of more than 7 g of fat per day in faeces [6] (plus morphological changes). Four of them had diabetes but no signs of peripheral vascular disease, and seven had enzyme substitution. The patients with residual pancreatic exocrine function had no steatorrhoea and meal stimulated intraduodenal lipase concentration far over 10% of lower normal limit (plus morphological changes) and had no other known gastrointestinal disorder, and no diabetes or peripheral vascular disease. The controls had no known gastrointestinal disease and were not taking any kind of medication.
All participants gave written informed consent to take part in the study, which was approved by the Regional Research Ethics Committee (KA 0129).
The ultrasound examinations were performed with a Philips HDI 5000 Sono CT unit (Philips Medical Systems, Bothell, WA). The SMA was examined in its long axis in the sagittal plane. The sampling cursor was placed within the diameter of the vessel, 2–3 cm distal to its origin, and the angle between the ultrasound beam and the SMA was kept smaller than 60°. The resistive index (RI) was calculated in accordance with the formula: peak-systolic velocity minus end-diastolic velocity divided by the peak-systolic velocity [7]. Each RI value is the average of three measurements.
To monitor gastric emptying the antrum was localized on a sagittal image in front of the superior mesenteric vein [8]. The image was frozen and the antral area was measured by means of the built-in calliper system. After the meal the antral area was determined at 5–10 min intervals until the area approached baseline, and the time from the meal until the area had decreased to 150% of baseline was used as surrogate expression of gastric emptying time [8].
Patients and healthy volunteers were examined in random order. Any pancreatic enzyme substitution was discontinued for 72 h before the study. The examination commenced after an overnight fast, with the subjects resting in the supine position for 45 min. RI in the SMA was recorded at least twice during the last 30 min before the meal and the baseline antral area was determined. The subjects then ingested a test meal consisting of 74.8 g NAN 1 (Nestlé Danmark A/S), containing 5.9% fat, 2.3% protein, and 11.6% carbohydrate, in 300 ml of water, with a total energy load of 1598 kJ, and SMA flow characteristics were recorded five times at 15 min intervals. Antral area was monitored as described. In most subjects, gastric emptying was not complete after 80 min. In these situations antral area was monitored for an additional 20 min.
For the data analysis, we calculated the difference between baseline RI and the mean of the five post-meal RI determinations in each participant. This difference thus expresses the integrated RI response to the test meal. Results were analysed for statistical significance using the Mann-Whitney two-sample rank sum test for unpaired data and Wilcoxon test for paired data. The Jonckheere-Terpstra test for ordered alternatives [9] was used to test the hypothesis that the postprandial shift in RI would be smaller with poorer exocrine function. Results are expressed as medians and ranges, and p<0.05 was considered statistically significant.
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Results
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The fasting RI was significantly lower in patients with exocrine insufficiency and in patients with reduced exocrine function, median values being 0.82 in both groups as compared with 0.85 in healthy volunteers, p = 0.028 and p = 0.0030, respectively (Table 2, Figure 1).
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Table 2. Median resistive index(RI) in the superior mesenteric artery before and after standard meal and antral emptying time after meal in eight patients with chronic pancreatitis and exocrine insufficiency, eight patients with chronic pancreatitis and preserved exocrine function and in eight healthy control persons
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Figure 1. Fasting resistance index(RI) in the superior mesenteric artery in eight patients with chronic pancreatitis and exocrine insufficiency, eight patients with chronic pancreatitis without manifest insufficiency and in eight healthy control persons.
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After the test meal, the RI decreased less in patients without and with residual exocrine function, 0.055 and 0.072, respectively, compared with controls, 0.099 (Table 2
, Figures 2 and 3). The difference between patients with exocrine insufficiency and controls was statistically significant, p = 0.0047, indicating less postprandial increase in mesenteric blood flow in exocrine insufficiency, whereas there was no significant difference between patients with residual exocrine function and the control group. There was a significant trend for less postprandial decrease in RI (less decrease in downstream circulatory resistance) from controls through patients with chronic pancreatitis without clinical insufficiency to patients with manifest pancreatic insufficiency (p = 0.0036, Figure 3).
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Figure 3. Difference between fasting and postprandial resistance index(RI) in the superior mesenteric artery in eight patients with chronic pancreatitis and exocrine insufficiency, eight patients with chronic pancreatitis without manifest insufficiency and in eight healthy control persons.
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There was no difference in the mean antral emptying time between the three groups (Table 2).
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Discussion
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We used RI to characterize downstream circulatory resistance in the SMA. It is calculated from two Doppler shift frequencies measured at the same image, and is independent of the angle of insonation. The RI is shown to increase linearly with the peripheral resistance at a constant pressure [7, 10]. It therefore makes sense that RI in the SMA has been reported significantly lower in active than in inactive ulcerative colitis [11] and Crohn's disease [12].
Median fasting RI in our control persons was 0.85 which is in agreement with results from other studies [11, 12]. Unexpectedly, both patients with chronic pancreatitis and patients with pancreatic insufficiency had significantly lower fasting RI in the SMA than controls, 0.82 in both groups. This suggests a more dilated vascular bed peripherally in the SMA territory in the fasting state in patients with chronic pancreatitis. To our knowledge this has not been previously reported, and further studies are needed to confirm this incidental observation. It could be speculated that in chronic pancreatitis the mechanisms that regulate the flow in the SMA are adapted to a weaker stimulus from the digested food components.
After the meal, RI decreased less (downstream resistance decreased less) in patients with exocrine insufficiency compared with patients with preserved exocrine function and with healthy controls (Figure 2). This lower effect of a meal on the blood flow in SMA in patients with exocrine insufficiency has not been demonstrated before. The test meal contained protein, fat and carbohydrate. All three components increase the blood flow in SMA after isocaloric and iso-osmotic loads into the duodenum [13]. In a recent study, instillation into the duodenum of free fatty acids (product of hydrolysis of triglycerides) increased SMA blood flow in normal subjects [1] to the same degree as we observed in the present study using a mixed test meal. Our results indicate that digestive products are more active in modulating SMA blood flow than undigested food. This could be due to increased release of vasoactive gastrointestinal hormones such as glucagon-like peptide-2 (GLP-2) during intestinal absorption of digestive products [14].
Since fat in the duodenum provokes gallbladder emptying [15], another explanation for our findings could be that the bile rather than the food causes the vascular effects. However, intravenous cholecystokinin in doses known to induce gallbladder contraction causes no flow response in SMA [16], so luminal bile does not seem to be responsible for the increased flow. Also, it has been reported that the postprandial gastric motility in chronic pancreatitis is altered [17, 18] so that a difference in gastric emptying of the test meal could influence our results. We therefore monitored antral emptying and observed no significant difference in antral emptying rate between patients and controls.
Any practical consequences of our findings remain to be defined. The modestly lower fasting RI in chronic pancreatitis is not impressive, the difference between medians in patients and controls being 0.03, but the majority of patients (11 of 16) actually had RI levels below the lowest level in our control persons (Figure 1). If other studies confirm this observation, it might be considered worthwhile to determine RI in the SMA routinely in all fasting upper abdominal studies, or at least in studies without an obvious diagnosis. An unusually low RI would suggest undetected abdominal pathology like inflammatory bowel disease or chronic pancreatitis.
The study confirms our hypothesis of a reduced postprandial increase in SMA flow in patients with exocrine pancreatic insufficiency. Further studies are needed to evaluate whether the meal induced shift in RI in the SMA can be used in the diagnosis and monitoring of chronic pancreatitis. Such a test would have the virtue of being non-invasive, in contrast to the duodenal-tube-based measurement of meal-induced release of lipase.
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Acknowledgments
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This study was supported by grants from the Danish Hospital Foundation for medical research. Region of Copenhagen, The Faroe Islands and Greenland (15/03). Special thanks to Tove Laursen for technical support.
Received for publication January 11, 2006.
Revision received April 5, 2006.
Accepted for publication April 24, 2006.
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Abstract
Introduction
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