Detection of choledocholithiasis by EUS in acute
pancreatitis: a prospective evaluation in 100
consecutive patients
Chi-Leung Liu, MS, FRCS (Edin), FACS, Chung-Mau Lo, MS, FRACS, FRCS (Edin), FACS,
John Ka-Fat Chan, MB, BS, FRCR (UK), Ronnie Tung-Ping Poon, MS, FRCS (Edin),
Chi-Ming Lam, MS, FRCS, Sheung-Tat Fan, MD, MS, FRCS (Edin Glasg), FACS,
John Wong, PhD, FRACS, FRCS (Edin), FACS
Hong Kong, China
Background: ERCP is the standard for detection of choledocholithiasis in patients with acute biliary pancreatitis, and, if performed early, ERCP decreases morbidity. However, there are procedure-related complications. The aim of the present prospective study was to evaluate the ability of
EUS to detect choledocholithiasis in patients presenting with acute pancreatitis.
Methods: The study group comprised 100 consecutive patients who presented with acute pancreatitis. EUS, and immediately thereafter, ERCP were performed by separate blinded examiners within 24 hours of admission. The diagnostic accuracy of EUS in identifying gallbladder stones was
compared with that of transcutaneous US. The diagnostic accuracy of EUS in detecting choledocholithiasis was then compared with that of US and ERCP based on the results of endoscopic
instrumentation of the bile duct after sphincterotomy.
Results: EUS was more sensitive than US in detecting gallbladder stones (100% vs. 84%, p <
0.005). The sensitivities of ERCP and EUS for choledocholithiasis were both 97%, and the overall
accuracies were 96% and 98%, respectively, with no significant difference. EUS detected the
absence of choledocholithiasis in 65 of 66 patients (specificity = 98%). Endosonographic examination was successful in all patients, whereas ERCP was unsuccessful in 5 patients (p > 0.05).
Post-endoscopic sphincterotomy bleeding developed in 4 patients; there was no EUS-related morbidity (p > 0.05).
Conclusion: EUS is more sensitive than US in detecting biliary stones in patients with acute pancreatitis. It is as accurate as ERCP in detecting choledocholithiasis. EUS can be used to select
patients with acute pancreatitis who require therapeutic ERCP, thus avoiding diagnostic ERCP and
its associated potential for complications in the majority of patients. (Gastrointest Endosc
2001;54:325-30.)
Acute pancreatitis can be a serious emergency
with significant morbidity and mortality. Biliary
stones are among the most common causes of acute
pancreatitis, although the reported incidence varies
among different populations. In patients with acute
pancreatitis, transcutaneous US is routinely performed to detect biliary stones and is highly accurate for the diagnosis of stones in the gallbladder.1-4
However, the sensitivity of US for detecting choledocholithiasis is limited.5-7 ERCP early in the
course of acute biliary pancreatitis, with endoscopic
Received June 9, 2000. For revision August 17, 2000. Accepted
May 25, 2001.
From the Departments of Surgery and Diagnostic Radiology,
University of Hong Kong Medical Centre, Queen Mary Hospital,
Hong Kong, China.
Reprint requests: Dr. Chi-Leung Liu, Department of Surgery,
University of Hong Kong Medical Centre, Queen Mary Hospital,
102 Pokfulam Rd., Hong Kong.
Copyright © 2001 by the American Society for Gastrointestinal
Endoscopy
0016-5107/2001/$35.00 + 0
37/1/117513
doi:10.1067/mge.2001.117513
VOLUME 54, NO. 3, 2001
sphincterotomy (ES) when choledocholithiasis is
detected, decreases morbidity rates for acute pancreatitis.8,9 However, ERCP has an associated morbidity rate of 3% to 6%.10,11 EUS is considered superior to US for imaging the extrahepatic biliary
system. Because of the use of higher frequencies
(7.5, 12, and 20 MHz) compared with those used for
US (2 to 5 MHz), EUS provides high-resolution
images of the layered structure of the gallbladder
wall and microlithiasis (0.5-2 mm) within the gallbladder.12 EUS has also been shown to be highly
accurate in the detection of choledocholithiasis.13,14
The aim of the present study was to prospectively
evaluate the ability of EUS to detect biliary stones
in patients with acute pancreatitis.
PATIENTS AND METHODS
The study comprised 100 consecutive patients (51 men,
49 women; median age 6l years; range 19-90 years) presenting with acute pancreatitis treated between November
1997 and March 1999 (Table 1). Thirty-eight patients
GASTROINTESTINAL ENDOSCOPY
325
C-L Liu, C-M Lo, J K-F Chan, et al.
EUS in acute pancreatitis
Table 1. Clinical characteristics of 100 patients
who presented with acute pancreatitis
Clinical factor
Age (y)
Gender ratio (male:female)
Duration of symptom (days)
Febrile on presentation
Clinical jaundice
Serum amylase on
admission (U/L)
Alkaline phosphatase on
admission (U/L)
Lactate dehydrogenase on
admission (U/L)
Total serum bilirubin on
admission (µmol/L)
Ranson’s score15 ≥3
A
Normal
range
61 (19-90)*
51:49
1 (0-5)*
16 (16%)†
14 (14%)†
1630 (355-2600)*
–
–
–
–
–
30-110
109 (30-813)*
49-138
488 (245-3070)*
197-401
29 (6-177)*
7-19
38 (38%)†
–
*Values expressed in median with range in parentheses.
†Number of patients with percentage in parentheses.
B
C
Figure 1. A, EUS image showing elongated stone in common bile duct. B, Endoscopic retrograde cholangiogram
showing stone in common bile duct. C, Endoscopic view
showing stone being removed from common bile duct with
basket after endoscopic sphincterotomy. S, Stone; CBD,
common bile duct; GB, gallbladder.
326
Value
GASTROINTESTINAL ENDOSCOPY
(38%) were diagnosed to have a severe attack of acute pancreatitis with a Ranson’s score of ≥3.15 Exclusion criteria
included a known diagnosis of recurrent pancreatitis related to chronic alcoholism or hyperlipidemia and post-ERCP
pancreatitis when that procedure was performed for reasons other than suspected biliary stones. Of the 100
patients, 15 had a previous diagnosis of gallstone disease
and 8 had undergone cholecystectomy. The diagnosis of
acute pancreatitis was based on acute abdominal pain and
a serum amylase level greater than 3 times the upper limit
of normal (normal <110 U/L). Biochemical analyses of
blood samples for liver and renal function, arterial blood
gases, calcium level, and lipid profiles, were performed
after admission. US was performed in all patients shortly
after admission; CT of the abdomen with contrast was performed on 27 patients. All US examinations were performed by expert radiologists with 2- to 4-MHz transcutaneous US probes (XP 10, Acuson, Mountain View, Calif.).
EUS and ERCP were both performed within 24 hours
of admission on all patients by endoscopists blinded to the
results of US. For EUS, patients were placed in the left
lateral position, an anesthetic spray was applied to the
pharynx, and sedation was obtained by intravenous
administration of diazepam and pethidine hydrochloride.
By using a 7.5-MHz echoendoscope (GF-UM20 or JFUM20, Olympus Optical Co., Ltd., Tokyo, Japan), US
images of the gallbladder and bile duct were obtained
with the instrument placed in the first and second parts
of duodenum and at the level of the distal antrum and
pylorus. Biliary tract images were obtained at different
angles by adjusting the position of the probe to minimize
examination “blind spots.” A persistent echogenic focus
with or without posterior acoustic shadowing was considered a biliary stone, microlithiasis, or sludge.
ERCP was performed immediately after EUS by a second endoscopist blinded to the EUS findings with the
patient still under conscious sedation. Once the ERCP
findings were reported by the second endoscopist, the
EUS findings were disclosed. If either test disclosed choVOLUME 54, NO. 3, 2001
EUS in acute pancreatitis
C-L Liu, C-M Lo, J K-F Chan, et al.
Table 2. Etiology of acute pancreatitis
Etiology
No. of patients (%)
Biliary
Gallstone present
Previous cholecystectomy
Hepatolithiasis without gallstones
Alcoholism
Hyperlipidemia
Idiopathic
Carcinoma of head of pancreas
Total
67
8
2
8
7
6
2
100
(67)
(8)
(2)
(8)
(7)
(6)
(2)
(100)
Table 4. Detection of choledocholithiasis in 100
patients with acute pancreatitis by ERCP
ERCP diagnosis of
choledocholithiasis
Final diagnosis of choledocholithiasis
(No. of patients)
Positive
Negative
Positive
Negative
31
1
3
60
ERCP was unsuccessful in 5 patients.
Table 5. Detection of choledocholithiasis in 100
patients with acute pancreatitis by EUS
Table 3. Sensitivity of transcutaneous US and
EUS in detection of cholelithiasis in 100 patients
with acute pancreatitis
Sensitivity
Cholecystolithiasis
Choledocholithiasis
US
EUS
p Value
56/67 (84%)
9/34 (26%)
67/67 (100%)
33/34 (97%)
<0.005
<0.001
ledocholithiasis, ES was performed (Fig. 1). By using
endoscopic instrumentation of the bile duct after ES as
the standard for the presence of choledocholithiasis, the
diagnostic accuracy of EUS was compared with that of US
and ERCP. If US, ERCP, and EUS did not detect choledocholithiasis, a presumptive diagnosis of no ductal
stones was made because it was considered to be ethically unacceptable to perform ES and instrumentation of the
bile duct to confirm the absence of stones.
Direct inspection of gallbladder content after cholecystectomy was used as the standard for the presence of gallstones. However, in a few patients who refused or were
considered unsuitable for cholecystectomy, a presumptive
diagnosis of gallstones was made when both US and EUS
showed one or more to be present. When US and EUS both
indicated the absence of gallstones, a presumptive diagnosis of no gallstones was made. All patients were closely
followed for recurrence of symptoms after endoscopic
clearance of choledocholithiasis with or without definitive
surgery for biliary stones (gallstones and hepatolithiasis).
Informed consents for the study and the endoscopic
procedures were obtained from all patients. The study
protocol was approved by the ethics committee of our hospital. Sensitivity, specificity, and overall accuracy of US,
EUS, and ERCP in the detection of biliary stones were
compared with the McNemar test. Statistical analysis was
performed with SPSS for Windows computer software
(SPSS Inc., Chicago, Ill.). A p value of < 0.05 was considered statistically significant.
RESULTS
The etiology of acute pancreatitis in the 100
patients is summarized in Table 2. Acute pancreatitis was biliary in origin in 77 patients; in 67 a diagnosis of gallstones was made. The presence of gallstones was confirmed by a direct inspection of the
VOLUME 54, NO. 3, 2001
EUS diagnosis of
choledocholithiasis
Final diagnosis of choledocholithiasis
(No. of patients)
Positive
Negative
Positive
Negative
33
1
1
65
Table 6. Comparison of transcutaneous US,
ERCP, and EUS in detection of choledocholithiasis in 100 patients with acute pancreatitis
Sensitivity*
Specificity†
Overall accuracy*
Successful examination†
Procedure-related morbidity†
US
ERCP
EUS
26%
100%
75%
100%
0%
97%
95%
96%
95%
4%
97%
98%
98%
100%
0%
*p < 0.001 comparing US vs. ERCP or EUS.
†p > 0.05 comparing all 3 diagnostic modalities.
gallbladder contents after cholecystectomy in 59 of
these patients. A presumptive diagnosis of gallstones
was made based on US and EUS in the remaining 8
patients; 5 refused cholecystectomy and 3 were considered unfit for surgery. US detected gallstones in
56 patients but missed them in 11 patients. Small
gallstones in these 11 patients were subsequently
detected by EUS and confirmed by cholecystectomy.
The median size of gallstones missed by US was 3
mm (range 1-6 mm). Thus, the sensitivity of US in
the detection of gallstones was 84%, significantly less
than that of EUS (100%, p < 0.005) (Table 3).
Examination of the distal common duct by US
was unsatisfactory in many cases because the duct
was frequently obscured by bowel distended with
gas. US detected ductal stones in 9 of the 34 patients
with a final diagnosis of choledocholithiasis, yielding a sensitivity of 26%, which was significantly less
than that of EUS (97%, p < 0.001) (Table 3). The
detection of choledocholithiasis by ERCP and EUS
is summarized in Tables 4 and 5. The sensitivity,
specificity, and overall accuracy of ERCP and EUS
in detecting choledocholithiasis were 97%, 95%, and
GASTROINTESTINAL ENDOSCOPY
327
C-L Liu, C-M Lo, J K-F Chan, et al.
Figure 2. Endoscopic view of major duodenal papilla showing impacted small pigmented stone (S) that escaped detection by EUS.
96% versus 97%, 98%, and 98%, respectively, with no
significant difference (Table 6). EUS examination
was successful in all patients, whereas ERCP was
unsuccessful in 5 patients (p > 0.05). In 2 of these 5
patients, EUS indicated the presence of choledocholithiasis. Repeat ERCPs were successful, and stones
were retrieved after ES. The remaining 3 patients
underwent operative cholangiography during subsequent cholecystectomy, and the absence of ductal
stones was confirmed. In 3 patients, ERCP was
falsely positive for choledocholithiasis. This was
probably related to small air bubbles introduced
during cannulation and injection of contrast. EUS
and ERCP both missed the diagnosis of choledocholithiasis in 1 patient, resulting in a sensitivity of
97% for both. A small stone impacted in the papilla
of 1 patient escaped detection by EUS (Fig. 2), the
findings being misinterpreted as an edematous
papilla. Except for this patient, EUS accurately
detected stones within the papilla in 6 other
patients. EUS detected hepatolithiasis in the left
lobe of the liver in 2 patients but missed hepatolithiasis in the right posterior segment in 1
patient. All 3 patients with hepatolithiasis had concomitant choledocholithiasis that was detected by
EUS. Hepatolithiasis was correctly diagnosed by
ERCP in all of these patients.
ERCP-related complications occurred in 4
patients (4%). All 4 had post-ES bleeding that
required a therapeutic endoscopic procedure during
the same endoscopy session (3 patients) or the next
day (1 patient). Among these patients, ERCP resulted in a false positive diagnosis of choledocholithiasis
in 1 patient. None of the patients required blood
transfusion. No EUS-related complication was
328
GASTROINTESTINAL ENDOSCOPY
EUS in acute pancreatitis
observed. The median duration of EUS was 14 minutes (range 8-23 minutes).
Although it was not possible to validate the presumptive absence of choledocholithiasis when both
ERCP and EUS were negative (false negativity by
both investigations), no patient in whom both studies were negative subsequently had symptoms
develop suggestive of retained stones after a median
follow-up of 22 months (range 12-29 months).
Similarly, although it was not possible to validate
the presumptive absence of gallstones because
cholecystectomy was not performed when both US
and EUS were negative for gallstones, no patient
with negative findings by both studies had clinical
evidence of gallstones after a median follow-up of 20
months (range 11-28 months).
In addition to the detection of biliary stones, EUS
was also helpful in determining the etiology of pancreatitis in 2 patients with carcinoma of the head of
pancreas (Table 2). These diagnoses were subsequently confirmed by histologic examination of surgical resection specimens.
DISCUSSION
The accuracy of US in detecting gallbladder
stones is high, with reported sensitivities ranging
from 92% to 96%.1-4 Traditionally, detection of gallstones in patients with acute pancreatitis has been
based primarily on US, but small gallstones are frequently encountered. Theoretically, small stones
pass more readily into the common duct and
through the papilla to cause acute pancreatitis. It
has been reported that when stones are less than 3
mm in diameter or are located in the gallbladder
infundibulum, the sensitivity of US is only 65%.16 A
recent study of the accuracy of US in detecting gallstones in 946 patients also found a false negative
rate of 1.3%.4 Although accuracy in gallstone detection in patients with acute pancreatitis can be
improved by repeating US at a later time, gallstones
can still elude detection in a sizable number of
patients.17 EUS, with its high-image resolution and
close proximity to the biliary system during examination, is considered superior to US for gallbladder
imaging. A study of 45 patients with clinically suspected biliary stones but with at least 2 normal US
examinations found that EUS detected evidence of
stones in the gallbladder of 26 patients.18 In the
present study, the sensitivity of US in detecting
cholelithiasis was only 84% and was inferior to that
of EUS (100%, p < 0.005). However, a limitation of
the present study was that the standard for absence
of gallstone included the EUS examination.
Nevertheless, none of the patients evaluated in this
way had clinical evidence of gallstones on follow-up.
VOLUME 54, NO. 3, 2001
EUS in acute pancreatitis
With its high accuracy for detection of microlithiasis within the gallbladder, EUS can play a role in
the identification of biliary causes of “idiopathic”
pancreatitis. In a recent study of 89 patients presenting with acute pancreatitis, EUS detected occult
biliary stones in 14 (78%) of 18 patients with a diagnosis of idiopathic pancreatitis by conventional radiologic methods; 18% of all cases of biliary pancreatitis were diagnosed by EUS alone.19 When a biliary
cause is identified, treatment can be initiated early,
thereby reducing the risk of recurrent pancreatitis
and its associated morbidity and mortality.
In addition to its sensitivity for detection of occult
cholelithiasis, EUS can also accurately detect choledocholithiasis.13,14 EUS is reported to have a significantly higher sensitivity (96%) than US (63%) or
CT (71%) in detecting choledocholithiasis with sensitivity unaffected by stone size or bile duct diameter.20 In addition, EUS performed before cholecystectomy can aid in the accurate selection of patients
with choledocholithiasis for surgical exploration of
the duct.21 In patients with acute biliary pancreatitis, EUS performed just before ERCP can aid in the
selection of patients for therapeutic endoscopic
intervention, thereby obviating the need for diagnostic ERCP with its potential risks in at least 50%
of patients. In the present study, EUS demonstrated
the absence of choledocholithiasis in 65 of 66
patients with a specificity of 98% (Table 5). In fact,
in one patient with post-ES bleeding, ERCP resulted in a false positive diagnosis of choledocholithiasis. Thus, this complication could potentially have
been avoided by EUS. EUS is less invasive and its
use can prevent repeated unsuccessful attempts at
cannulation during ERCP, which can potentially
worsen acute pancreatitis.
Despite the advantages of EUS in relation to
ERCP, EUS has limitations when investigating the
possibility of choledocholithiasis in patients presenting with acute pancreatitis. In our area of the
world, the bile duct in these patients frequently harbors small, soft, pigmented stones that may not cast
an echogenic shadow. Thus, detection by EUS of
such a stone impacted at the papilla can be difficult.
In the present study, the correct diagnosis in 1 of the
7 patients who had an impacted stone was missed
by EUS. Later in the course of the study our technique was modified to include a side-view echoendoscope (JF-UM20, Olympus) instead of an
oblique-viewing instrument. This allowed direct
inspection of the papilla. Another drawback of EUS
is that it is difficult to examine the intrahepatic biliary tree. In our geographic region, hepatolithiasis
accounts for acute pancreatitis in a small number of
patients (3 patients in the present study).22
VOLUME 54, NO. 3, 2001
C-L Liu, C-M Lo, J K-F Chan, et al.
Intrahepatic ductal stones can easily be missed in
this group of patients; EUS failed to show such
stones in 1 patient in the present study. Thus, other
imaging modalities (US, CT, or ERCP) may be
required for the diagnosis of hepatolithiasis in
patients with acute pancreatitis.
EUS could potentially provide prognostic information in patients with acute pancreatitis. Schoefer
et al.23 preliminarily reported data from a prospective study of the prognostic value of EUS in 31
patients with acute pancreatitis. A numerical EUS
score was developed based on EUS findings (organ
size, aspect of the outer margin of pancreas,
echogenicity, location, and the extent of peripancreatic fluid). The EUS score correlated significantly
with the duration of hospital stay, duration of fever,
length of intensive care, and CT prognostic index. In
another prospective study,24 there appeared to be a
relationship between EUS findings of peripancreatic fluid and echogenicity of the pancreas and mean
hospital stay. However, the timing of EUS for documentation of pancreatic lesions in this study is
unclear. Although these data are intriguing, further
studies are required to evaluate the prognostic role
of EUS in patients with acute pancreatitis.
Magnetic resonance imaging (MRI) has been
shown to be highly accurate in detecting choledocholithiasis (sensitivity 85% to 100%).25-27 MRI has also
been reported as useful in patients with acute pancreatitis by providing a severity index and because it
is helpful in differentiating interstitial pancreatitis
from necrotizing pancreatitis.28 Like EUS, MRI
could in theory detect choledocholithiasis in patients
presenting with acute pancreatitis and thereby aid
in the selection of patients for therapeutic ERCP.
However, the accuracy of MRI in the detection of choledocholithiasis in the setting of acute pancreatitis
has not been fully documented. Compared with MRI,
EUS is more readily available in our hospital, especially within the first 24 hours after admission.
Moreover, if choledocholithiasis is detected by EUS,
ERCP with ES can be performed immediately while
the patient is still sedated. Further study of the
cost-effectiveness of these 2 modalities in the detection of choledocholithiasis in patients with acute
pancreatitis is needed.
The present study was performed in a region
where the incidence of pigmented stones is high.
Over 70% of our patients presenting with acute pancreatitis have biliary stones. This figure is much
higher than that for Western countries. Therefore,
the results of the present study may not be generally applicable to other regions. However, because the
frequency of choledocholithiasis is lower among
Western populations, an accurate but less invasive
GASTROINTESTINAL ENDOSCOPY
329
C-L Liu, C-M Lo, J K-F Chan, et al.
diagnostic modality for confirmation of the presence
of bile duct stones prior to therapeutic ERCP would
be of even greater value. Whether EUS or MRI will
become the investigation of choice may depend on
the local availability of expertise and facilities.
In summary, EUS is more sensitive than US in
detecting cholelithiasis and choledocholithiasis in
patients with acute pancreatitis. Moreover, EUS is
as accurate as ERCP in detecting choledocholithiasis. EUS can be used to select patients with acute
pancreatitis for therapeutic ERCP, thus avoiding
diagnostic ERCP with its greater potential for morbidity in a majority of patients. The potential benefit and the cost-effectiveness of this new endoscopic
approach require further investigation.
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