Original Article
Biliary Sludge as a Cause of Acute Pancreatitis
N Engl J Med 1992; 326:589-593February 27, 1992
- Abstract
- Abstract
Background.
In about 20 to 40 percent of cases of acute pancreatitis, no cause can be found, and these are labeled idiopathic. In this study, we sought to determine the frequency with which patients with acute idiopathic pancreatitis have biliary sludge, a suspension of cholesterol monohydrate crystals or calcium bilirubinate granules that is found predominantly in the gallbladder.
Methods.
Between 1980 and 1988, we prospectively studied 86 patients who had acute pancreatitis. In patients with no known cause of pancreatitis and no ultrasonographic evidence of gallstones or dilatation of the biliary ducts, we determined how often biliary sludge was present and its subsequent fate by repeated microscopical examinations of bile samples and abdominal ultrasonography. The outcome of patients treated by cholecystectomy or papillotomy was compared with that of untreated patients.
Results.
The pancreatitis was considered idiopathic in 31 of the 86 patients (36 percent), of whom 23 had microscopical evidence of biliary sludge. Biliary sludge was detected by ultrasonography in only 11 of the 23 patients (48 percent). The sludge detected by ultrasonography was composed of calcium bilirubinate granules in 10 and cholesterol monohydrate crystals in 1 (P = 0.003). Calcium bilirubinate granules were found more frequently in men (nine men vs. four women, P<0.001). Of the 21 patients in whom biliary sludge was the only finding (2 patients also had dilated bile ducts when restudied), the 6 treated by cholecystectomy and the 4 treated by papillotomy had fewer recurrences of acute pancreatitis during follow-up (up to seven years) than the 11 untreated patients (P = 0.011). The presence of biliary sludge appeared to increase the likelihood of recurrent attacks of pancreatitis (P = 0.020).
Conclusions.
Biliary sludge is an underestimated cause of acute idiopathic pancreatitis. (N Engl J Med 1992;326:589–93.)
Media in This Article
Figure 1
Ultrasonographic Features of Biliary Sludge.Figure 2
Microscopical Features (×200) of Biliary Sludge Containing Predominantly Cholesterol Crystals (Panel A) and Predominantly Calcium Bilirubinate Granules (Panel B).Article Activity
- Article
THE most common causes of acute pancreatitis are alcohol abuse and gallstone disease, which together account for nearly 70 percent of cases. Fewer than 2 percent of the cases of acute pancreatitis are caused by hypercalcemia, hyperlipidemia, and drugs. The remaining cases are idiopathic.1 2 3 Pancreatitis is associated with serious complications and a mortality rate that is linked to the cause of the disease. For alcoholic pancreatitis, the overall mortality is about 5 percent; for gallstone-associated and idiopathic pancreatitis, it is 10 to 25 percent.4
Acute idiopathic pancreatitis frequently occurs in association with pregnancy (acute pancreatitis of pregnancy), the administration of total parenteral nutrition, or major surgery (postoperative pancreatitis). Many patients with acute pancreatitis have precipitates commonly referred to as sludge in their gallbladder bile.5 6 7 Biliary sludge is defined as a suspension of cholesterol monohydrate crystals or calcium bilirubinate granules in bile and is found predominantly, although not exclusively, in the gallbladder. Several lines of evidence have suggested that these precipitates in the gallbladder are involved in idiopathic pancreatitis. Tissue specimens obtained during cholecystectomy from patients with acute idiopathic pancreatitis contain precipitates of various descriptions in approximately 60 percent of cases.8 9 10 Microscopy of bile obtained from duodenal fluid showed crystals in 30 percent of cases.11 Careful sieving of feces within 72 hours after the subsidence of an attack of acute idiopathic pancreatitis revealed concretions (presumed to be biliary in origin) of various dimensions.10 11 12 13 In all these cases, radiologic methods had failed to detect gallstones. There are, however, at least two problems in retrospectively implicating precipitates in bile as a cause of acute pancreatitis. First, biliary sludge may develop in a patient who cannot eat. Second, swelling of the head of the pancreas may lead to obstruction of the common bile duct. Bile stasis predisposes patients to the formation of biliary sludge,14 and distal obstruction of the common bile duct is associated with the ultrasonographic finding of biliary sludge.15
We prospectively studied a group of patients hospitalized for acute pancreatitis and identified those with unexplained or idiopathic pancreatitis. We then used microscopical analysis of bile and ultrasonography to determine the frequency of biliary sludge in this group of patients. We also attempted to assess the relation of biliary sludge to subsequent attacks of acute pancreatitis.
Methods
Selection of Patients
We studied all 86 patients with acute pancreatitis who were treated at the University of Auckland Medical Center in Auckland, New Zealand, or the Veterans Affairs Medical Center in Seattle between July 1980 and September 1988. Patients were considered to have acute pancreatitis if they had abdominal pain and one or more of the following abnormalities: a serum amylase concentration above 800,000 U per liter (more than four times the upper limit of normal), a serum lipase concentration above 200,000 U per liter (more than three times the upper limit of normal), and pancreatic swelling, phlegmon, or necrosis demonstrated by CT. Patients were considered to have acute idiopathic pancreatitis if they had no history of alcohol abuse (ingestion of more than 80 g of ethanol per day for men and more than 60 g of ethanol per day for women); no history of having received a thiazide diuretic, corticosteroid, azathioprine, or cyclosporine; no hypercalcemia or hypertriglyceridemia; and no ultrasonographic evidence of gallstones or dilatation of the intrahepatic or extrahepatic biliary ducts. All 86 patients had ultrasonography, and most patients subsequently had either endoscopic retrograde cholangiopancreatography or additional abdominal CT scans to confirm that the common bile duct was not obstructed. The study protocol was approved by the ethics committee for human subjects, and informed consent was obtained from all patients.
Study Design
Thirty-one patients were considered to have acute idiopathic pancreatitis, and all had a sample of bile examined by polarizing microscopy. Bile was obtained during endoscopic retrograde cholangiopancreatography in 15 patients. In 16 patients, bile was aspirated through a soft feeding tube placed beforehand into the duodenum, after intravenous administration of 100 units of cholecystokinin. The bile samples were obtained during convalescence, three to six weeks after the onset of pancreatitis.
The patients underwent abdominal ultrasonography at entry into the study and every six months thereafter, as well as during any subsequent attack of pancreatitis. The duration of follow-up ranged from six months to seven years, with a mean of four years. Six patients were treated with cholecystectomy, and four with endoscopic papillotomy. We emphasize that the study was not designed as a controlled trial of treatment as compared with no treatment of acute idiopathic pancreatitis. Nevertheless, because of the length of follow-up, we were able to assess the effect of treatment on the subsequent relapse rate.
Definition and Diagnosis of Biliary Sludge
Biliary sludge consists of a suspension of precipitates of cholesterol monohydrate crystals or calcium bilirubinate granules in bile. These precipitates can be identified by microscopical examination of bile samples or detected by ultrasonography. Since ultrasonography has a much lower resolution than microscopy, and since ultrasonography detects echoes from the precipitates but cannot determine their chemical composition, the ultimate decision about the presence or absence of biliary sludge in each patient was based on microscopical findings.
Imaging Criteria
Gallbladder sludge was considered to be present on ultrasonography if mobile, low-amplitude echoes were seen in the lumen that layered in the most dependent part of the gallbladder and were not associated with shadowing16 , 17 (Fig. 1Figure 1
Ultrasonographic Features of Biliary Sludge.). Gallstones were characterized by high-amplitude echoes that were usually mobile and accompanied by postacoustic shadows. When both stones and sludge were found in the gallbladder, the patient was excluded from the study. The ultrasonographers were not aware of the results of the microscopical examination of bile.Morphologic Criteria
Sludge was considered to be present morphologically if sediment was found that did not assume a fixed form or shape. If the sediment clumped, it could be dispersed by agitation or minimal digital pressure. To be considered gallstones, the sediment had to be in the form of stable concretions that were 2 mm or more in diameter and that could not be dispersed by agitation or digital pressure.
Microscopical Examination of Bile Samples
Samples of bile were obtained, immediately centrifuged at 4000×g for 10 minutes, and examined with a polarizing microscope (Nikon EFI) equipped with a heating stage.15 Cholesterol monohydrate crystals were identified on the basis of their rhomboidal shape and by their birefringence under cross-polarization (Fig. 2Figure 2
Microscopical Features (×200) of Biliary Sludge Containing Predominantly Cholesterol Crystals (Panel A) and Predominantly Calcium Bilirubinate Granules (Panel B).A). Calcium bilirubinate granules were identified on the basis of reddish-brown color (Fig. 2B). Samples were considered positive for cholesterol or calcium bilirubinate granules if there were five or more crystals or clumps per slide. At least three slides were examined for each sample. Because the concentration of bile varied from sample to sample and because of contamination with other secretions in the duodenum, no attempt was made to grade the abundance of crystals or clumps.The samples of bile were examined by one of the investigators, who was not aware of the patients' clinical condition. Each sample was compared with positive- and negative-control slides containing cholesterol monohydrate crystals and calcium bilirubinate granules; the control specimens had been processed from frozen samples. In addition, the concentrations of cholesterol, phospholipids, bilirubin, calcium, and bile salts were determined in each sample. Gallstones were classified as cholesterol or pigment gallstones, according to previously described methods.15
Results
The clinical characteristics of the 86 patients who were hospitalized with acute pancreatitis are summarized in Table 1Table 1
Causes of Acute Pancreatitis in and Clinical Features of the 86 Study Patients.. Twelve patients (14 percent) had a history of alcohol abuse, 43 (50 percent) had gallstones, and 31 (36 percent) had idiopathic pancreatitis. Three of the 14 patients with a history of alcohol abuse had ultrasonographic evidence of gallbladder sludge, but not microscopical evidence. Twenty-three of the 31 patients (74 percent) with acute idiopathic pancreatitis had biliary sludge demonstrable by ultrasonography, microscopical examination of bile, or both.Two patients with acute idiopathic pancreatitis who had biliary sludge were excluded because dilated bile ducts were detected by endoscopic retrograde cholangiopancreatography and CT at the time bile was sampled during convalescence. Of the 29 remaining patients, 21 had microscopical evidence of biliary sludge. Nine of these 21 patients (8 women and 1 man) had predominantly cholesterol crystals. Their mean (±SD) age was 41±11 years. The other 12 patients (4 women and 8 men) had primarily calcium bilirubinate granules. Their mean age was 67±13 years. Calcium bilirubinate crystals were more common in men than in women (nine men vs. four women, P<0.001). Eleven of the 21 patients (52 percent) had ultrasonographic evidence of gallbladder sludge (Table 2Table 2
Ultrasonographic and Microscopical Features of Biliary Sludge in 21 Patients with Acute Idiopathic Pancreatitis without Obstruction of the Common Bile Duct.*). Ultrasonography was more likely to detect calcium bilirubinate granules than cholesterol crystals (10 patients vs. 1 patient; P = 0.003 by Fisher's exact test).Two of the eight patients with acute idiopathic pancreatitis who did not have biliary sludge had a second attack of acute pancreatitis during follow-up; one of the two also had ultrasonographic evidence of gallbladder sludge. Bile samples were not examined microscopically in this patient during the recurrence.
Of the 21 patients who had biliary sludge but no large-duct obstruction, 6 underwent cholecystectomy and operative cholangiography, with or without exploration of the common bile duct. One patient was operated on during the first admission, and five were operated on after a second attack of acute pancreatitis. During follow-up, none of the patients had further episodes of acute pancreatitis after cholecystectomy, and none had biliary sludge in later bile samples studied microscopically. Four patients who had biliary sludge were treated by endoscopic papillotomy; one patient had the procedure during her first hospitalization, and the other three were operated on during subsequent attacks of acute pancreatitis. One of these four patients had another episode of acute pancreatitis after the operation. This patient had ultrasonographic and microscopical evidence of persistent biliary sludge.
Eleven of the 21 patients with biliary sludge did not undergo cholecystectomy or papillotomy. Eight of these patients had one or more subsequent attacks of acute pancreatitis. Four of these eight patients were found to have gallbladder sludge on subsequent ultrasound examinations, and gallstones developed in three during a three-year period. Nine of the 11 untreated patients had follow-up microscopical examinations of bile samples; all the samples contained biliary sludge.
The patients who underwent cholecystectomy or papillotomy had fewer recurrences of acute pancreatitis during follow-up than the untreated patients (P = 0.011 by Fisher's exact test). The presence or persistence of biliary sludge was significantly correlated with the risk of subsequent attacks of acute pancreatitis (P = 0.020 by Fisher's exact test).
The gallbladder contained sludge in all six patients who underwent cholecystectomy. Four had multiple small stones that were larger than 2 mm in diameter. The gallbladder bile had a mean (±SD) cholesterol concentration of 16±6 mmol per liter, a phospholipid concentration of 47 ± 11 mmol per liter, and a bile-salt concentration of 171 ±46 mmol per liter, with a total lipid density of 109±38 g per liter and an adjusted cholesterol saturation index of 1.2±0.3. These values did not differ significantly from those found by us in normal subjects and patients with gallstones in previous studies.15 , 18
Discussion
In our study, 31 of 86 patients with acute pancreatitis (36 percent) had what is generally considered acute idiopathic pancreatitis, and the majority (67 percent) had biliary sludge. Three of the 14 alcoholic patients also had ultrasonographic evidence of gallbladder sludge, but because of the presence of alcoholism, the disease could not be classified as idiopathic. We found that biliary sludge was often present without obstruction of large bile ducts. Whether the biliary sludge was causally associated with the pancreatitis is not clear, but its presence was predictive of recurrences of acute pancreatitis.
Ultrasonography is a useful, simple, and noninvasive diagnostic technique in patients with an acute abdomen. However, it is less sensitive in the detection of biliary sludge than microscopical analysis of bile. The fact that patients probably should not undergo duodenal intubation with cholecystokinin infusion during the active phase of acute pancreatitis limits the diagnostic value of microscopy. It may be helpful to begin with cholecystography (with patients sitting during the study) before proceeding to duodenal aspiration and microscopy. In this study, in which we systematically compared ultrasonography and microscopy, 10 of 21 patients who had microscopical evidence of biliary sludge had a negative ultrasound examination. Thus, ultrasonography had a false negative rate of 48 percent. Ultrasonography did not detect small stones in four of the six patients with biliary sludge who underwent cholecystectomy. Ultrasonography was more likely to detect sludge composed of calcium bilirubinate granules than sludge composed of cholesterol monohydrate crystals.
Abnormalities of hepatic bile secretion, as well as changes in the contractile and mucosal function of the gallbladder, contribute to the pathogenetic process resulting in biliary sludge.19 , 20 The clinical outcome of patients who have gallbladder sludge is unclear. As in this study, others have found that in some patients biliary sludge can cause symptoms or eventually evolve into gallstones.5 6 7 , 21 We and others have suggested that these precipitates can either dissolve spontaneously or be discharged into the small intestine, and they may also recur.5 , 7 , 21 22 23 Biliary sludge may also be causally related to papillitis, papillary spasm, or papillary stenosis.24 As is the case with gallstones, gallbladder sludge does not necessarily produce symptoms. When gallbladder sludge is associated with biliary pain or recurrent attacks of acute pancreatitis, however, it should be treated in the same way as gallstones. Our findings indicate that the course of pancreatitis associated with biliary sludge is similar to that of gallstone-associated pancreatitis, and both have a high risk of recurrence. Ros et al.25 made similar observations; in their study, biliary sludge accounted for approximately 67 percent of all cases of acute idiopathic pancreatitis. Moreover, in our study cholecystectomy virtually eliminated subsequent attacks.
There are limitations to the interpretation of our findings. The possibility that pancreatitis itself might have modified the contents of the gallbladder cannot be excluded. However, we did attempt to exclude patients with obstruction of the common bile duct with endoscopic retrograde cholangiopancreatography and CT, and the follow-up data suggested that the sludge was a cause and not a result of acute pancreatitis.
We believe that the causative role of biliary sludge in acute pancreatitis is underestimated. We also believe that biliary sludge should be excluded as a cause before a diagnosis of idiopathic pancreatitis is made. The presence of sludge has important implications for the treatment and prognosis of acute pancreatitis.
Supported in part by the Medical Research Service of the Department of Veterans Affairs.
We are indebted to Paul Beeson, M.D., and Benjamin Lipsky, M.D., for their assistance in reviewing the manuscript.
Source Information
From the Department of Medicine, University of Washington, Seattle (S.P.L., H.Z.P.), and the Department of Medicine, University of Auckland, Auckland, New Zealand (J.F.N.). Address reprint requests to Dr. Lee at the Department of Medicine (111GI), VA Medical Center, 1660 S. Columbian Way, Seattle, WA 98108.
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