Is Routine Intraoperative Cholangiogram Necessary in Patients With Mild Acute Biliary Pancreatitis Undergoing Index Admission Cholecystectomy?

Abstract

Background: There is controversy about whether intraoperative cholangiogram (IOC) should be performed routinely during laparoscopic cholecystectomy for patients with acute biliary pancreatitis, given significant false positive and negative rates and increased resource utilization. The aim of this study was to clarify the role of IOC in cases of mild biliary pancreatitis in patients undergoing index admission cholecystectomy, its impact on patient outcomes, and the impact of blood tests, imaging, and preoperative intervention on the detection of choledocholithiasis.

Methods: A retrospective review of all patients presenting with acute mild biliary pancreatitis between January 2006 and December 2019 was conducted. Data collected included patient demographics, serum chemistry, IOC, and Endoscopic Retrograde Cholangiopancreatography (ERCP) findings, imaging findings, length of stay, operative length, and long-term follow-up outcomes.

Results: 284 patients met the inclusion criteria for the study. The overall false positive IOC rate was 7.4%. Worsening bilirubin trend was a positive predictive value (PPV) for positive IOC and ERCP outcomes with a relative risk of 2.93 (P < .01) and 2.32 (P = .013), respectively. Improving preoperative bilirubin trend had a significant negative predictive value in IOC with a relative risk of .59 (P = .02). Positive IOC was shown to significantly increase operative length with a relative risk of 2.03 (P < .001).

Discussion: A rising preoperative bilirubin is a predictor of a positive IOC and patients with normalizing bilirubin levels or a preoperative ERCP are less likely to have choledocholithiasis. These features may be used to select patients that would benefit from an IOC for index admission cholecystectomy.

Keywords

intraoperative cholangiogram biliary pancreatitis cholecystectomy

Key Takeaways

• In patients with mild biliary pancreatitis, a rising preoperative bilirubin is a predictor of a positive IOC and patients with normalizing bilirubin levels or a preoperative ERCP are less likely to have choledocholithiasis.

• These features may be used to select patients that would benefit from an IOC for index admission cholecystectomy following acute mild biliary pancreatitis.

Background

Acute biliary pancreatitis is a common reason for emergency surgical admission associated with significant morbidity, mortality, and high health care costs.^1,2 Laparoscopic cholecystectomy is recommended at the index admission in these patients to prevent recurrent episodes of biliary pancreatitis or associated biliary complications.^1-5 The use of intraoperative cholangiogram (IOC) is routine in Australia and occurs in approximately 80% of all cases; however, this varies in other countries and there remains controversy about whether IOC should be performed routinely or on a more selective basis given significant false positive and negative rates, increased operating theater time, and resource utilization with an estimated average cost of 15,000 USD p. a. per surgeon.^6-9 This is particularly relevant in resource poor countries. The purpose of the IOC is to detect choledocholithiasis in order to prevent further episodes of biliary pancreatitis in addition to defining the biliary anatomy, therefore, aiming to prevent or reduce the severity of bile duct injuries.^10,11 A recent meta-analysis did not show any statistically significant difference in choledocholithiasis detection rates or bile duct injury rates in the routine vs the selective IOC groups, including those who had previous biliary pancreatitis.¹² There are no universally accepted criteria for selective IOC but a history of acute pancreatitis has been considered an indication to detect residual choledocholithiasis; however, another study suggested that IOC is unnecessary in patients with mild biliary pancreatitis and normalizing bilirubin levels.¹

Our hypothesis is that IOC is not required in patients undergoing index admission cholecystectomy if they have a normalizing bilirubin or a preoperative ERCP. Therefore, the aim of this study is to clarify the role of IOC in patients with mild biliary pancreatitis undergoing index admission cholecystectomy, to determine if there are preoperative variables that predict the presence of choledocholithiasis and the impact of routine IOC on outcomes. We investigated the impact of liver function tests, common bile duct diameter on ultrasound and preoperative Endoscopic Retrograde Cholangiopancreatography (ERCP) on the incidence of choledocholithiasis detection on IOC and the impact of IOC findings on patient outcomes.

Methods

A retrospective review of all patients presenting with acute biliary pancreatitis to a tertiary level hospital between January 2006 and December 2019 was conducted. Patients with mild acute biliary pancreatitis who underwent index admission laparoscopic cholecystectomy formed the study population. These patients were managed by the acute surgical unit during the admission and were operated on by the acute care surgeon or surgical trainees under their direct supervision. A routine IOC was attempted for all laparoscopic cholecystectomies.

Clinical records including serum chemistry, progress notes, histopathology results, imaging, anesthetic preoperative assessment, discharge summaries, and operation records were reviewed. Data collected included patient demographic data, admission, and preoperative liver function tests (LFTs)—including bilirubin level (Br), aspartate aminotransferase level (AST) and alanine aminotransferase level (ALT), white cell count (WCC), C-reactive protein (CRP), previous surgical history, operative cholangiogram findings, preoperative and postoperative ERCP findings, imaging findings, length of stay, operative length, and long-term follow-up outcomes including readmission rates and procedural complications.

Inclusion criteria for the study were patients over the age of 18 who underwent cholecystectomy during their index admission for mild biliary pancreatitis, and who had at least 2 sets of biochemical markers available for assessment (admission and preoperative). Exclusion criteria for the study was any patient under the age of 18 who did not undergo cholecystectomy during index admission and who did not have adequate data available (including operative details, IOC and ERCP outcomes and at least 2 sets of biochemical markers for comparison).

Acute pancreatitis was diagnosed using the Atlanta criteria and a diagnosis of biliary etiology was made based on imaging and/or biochemical features and in the absence of another cause being identified. MRCP was used selectively in patients suspected to have choledocholithiasis, due to limited availability, with its use increasing over the study period.

Patients underwent ERCP preoperatively if a stone was identified in the common bile duct on preoperative imaging, or if there were elevated bilirubin levels in conjunction with a dilated biliary system. The revised Atlanta classification was used to determine severity of pancreatitis.¹³ The trend in biochemical markers were determined by a change in value from the first test to the second test (a decrease in value was determined to be improving, an increase in value was determined to be worsening and a static value was when there was no change, or a change within 1-2 units).

Data was collated using Microsoft excel and was analyzed using a statistical software (Stata version 16, StataCorp LLC). Results were to be obtained from multiple univariable log-binomial regressions of the collected variables. Relative risks with associated 95% confidence intervals were reported, along with P-values.

Results

A total of 1802 patients presented with acute pancreatitis during the study period. 781 patients were admitted with acute biliary pancreatitis and 284 met the inclusion criteria for the study (36.3%) (Figure 1). The incidence of biliary pancreatitis and percentage of patients undergoing index admission cholecystectomy is shown in Figure 2, which demonstrates generalized improved uptake in index admission cholecystectomy over time.

Of the included patients the majority were female (62.3%) with a mean age of 51.7 (SD 17.8). Average length of stay was 7.2 days (SD 4.1) and included time to operation, postoperative recovery, and time awaiting additional intervention such as ERCP. Mean operative time was 1.57 hours (SD .62) (Table 1).

Table 1.

Characteristics of Index Admission Laparoscopic Cholecystectomies From 2006 to 2019.

	Total	Male	Female
Sample size	284 (100%)	107 (37.7%)	177 (62.3%)

	Median	Range	Mean	SD
Age (years)	51	15-91	51.7	17.8
Length of stay (days)	7	0-27	7.2	4.1
Length of operation (hour)	1.43	.37-5.92	1.57	.62
CBD size (mm)	5	2-14	5.9	2.4

	Performed	Positive Finding	True Positive	Complication
Intraoperative cholangiogram	268 (94.0%)	58 (21.6%)	27 (10.1%)	4 (1.5%)

	Performed	Positive Finding	ERCP Complication
Preoperative ERCP	37 (13.0%)	26 (70.3%)	2 (5.4%)
Postoperative ERCP	30 (10.6%)	14 (46.7%)	2 (6.6%)

A total of 67 patients had either preoperative or postoperative ERCP (48% of ERCP preoperatively and 52% postoperatively). Two patients had both preoperative and postoperative ERCP. 37 patients had preoperative ERCP where choledocholithiasis was identified in 26 (70.3%) patients, and in these patients, the IOC showed persistent filling defects in 10 patients with 2 patients requiring postoperative ERCP. 8 patients (22%) had filling defects which were either flushed or monitored postoperatively (Table 1).

Two patients who underwent preoperative ERCP developed post-ERCP pancreatitis, and both had stones successfully retrieved. Two patients who underwent postoperative ERCP had significant GI bleeding, neither of whom were found to have choledocholithiasis.

Worsening bilirubin trend was a positive predictive value for positive ERCP (RR 2.32, P = .013), while GGT, ALT, WCC, and CRP were shown to be of no value in predicting the outcome of ERCP (Table 2). Static bilirubin levels on the other hand had no correlation with IOC or ERCP findings.

Table 2.

Association Between ERCP Finding and Worsening Serum Markers.

Serum Marker	Relative Risk^a	95% Confidence Interval		P-Value⁺
Bilirubin	2.32	1.20	4.49	.013
GGT	1.02	.49	2.14	.955
ALT	1.09	.42	2.84	.858
WCC	1.50	.63	3.58	.361
CRP	.85	.38	1.91	.697

Results obtained from multiple univariable log-binomial regressions with ERCP finding of stone as the dependent variable and worsening serum marker trends as the independent variable.

+ Bold denotes P-value <.05.

IOCs were performed routinely with a 94% success rate. 6% did not have a cholangiogram for various reasons including technical difficulty, contrast allergy, pregnancy, or a bile duct injury. A filling defect was reported in 58 patients (21.6%) by the surgeon undertaking the IOC. Of these, 30 patients went onto have postoperative ERCP at the index admission with confirmation of choledocholithiasis in 14 (46.5%) patients (Table 1). 16 (53.3%) were found to have a negative ERCP, suggesting either a false positive IOC or that the stone had passed without intervention, indicating a potentially unnecessary procedure. Of the remaining 28 patients (48.2%), 8 patients had small stones that were flushed intra-operatively and 2 had a laparoscopic bile duct exploration. In 5 patients, the filling defects were thought to be air bubbles with no further intervention. 13 patients were monitored with serial liver function test or MRCP with 3 of these patients going onto having an ERCP as an outpatient. Therefore, 27 (46%) patients had confirmed choledocholithiasis following a positive IOC or 10.1% of the overall patients who had an IOC (Table 1). The false positive rate following positive IOC was 36% (16 with negative ERCP and 5 patients with suspected “air bubbles”); therefore, an overall false positive rate was 7.4% for all patients who had IOC. One patient did not have an IOC due to a bile duct injury.

Worsening trend in bilirubin was the only positive predictive value for positive IOC outcome (RR 2.93, P < .01), while GGT, ALT, WCC, and CRP were not useful in predicting positive IOCs (Table 3). Improving preoperative bilirubin trend had a significant negative predictive value (RR .59, P = .02) (Table 4).

Table 3.

Association Between Intraoperative Cholangiogram Finding and Worsening Serum Markers.

Serum Marker	Relative Risk^a	95% Confidence Interval		P-Value⁺
Bilirubin	2.93	1.71	5.01	<.01
GGT	1.20	.70	2.05	.506
ALT	1.56	.83	2.90	.164
WCC	1.22	.59	2.54	.587
CRP	.96	.53	1.74	.889

^aResults obtained from multiple univariable log-binomial regressions with intraoperative cholangiogram finding of filling defect as the dependent variable and worsening serum marker trends as the independent variable.

+ Bold denotes P-value <.05.

Table 4.

Association Between Intraoperative Cholangiogram Finding and Improving Serum Markers.

Serum Marker	Relative Risk*	95% Confidence Interval		P-Value⁺
Bilirubin	.59	.36	.92	.020
GGT	1.07	.63	1.82	.808
ALT	.89	.54	1.48	.659
WCC	1.17	.74	1.84	.502
CRP	1.52	.96	2.39	.074

^aResults obtained from multiple univariable log-binomial regressions with intraoperative cholangiogram finding of filling defect as the dependent variable and improving serum marker trends as the independent variable.

+ Bold denotes P-value <.05.

Positive intraoperative cholangiogram was shown to significantly increase operative length (RR 2.03, P < .001) (Supplemental Table 5).

Of all the patients who underwent index admission cholecystectomy, 2 patients had a return to theater for bleeding and 2 patients had a bile duct injury or a bile leak.

There was no correlation found between CBD dilation and IOC or ERCP findings (Supplemental Table 6).

Discussion

Laparoscopic cholecystectomy is routinely performed as the gold standard in management of mild acute biliary pancreatitis.^1,2 It is recommended at the index admission and can be considered as early as day 2 following diagnosis.^1-3 The study shows that a significant number of patients did not proceed to an index admission cholecystectomy predominantly due to resource availability and patient preference to undergo operations within the private system or refusal to consent to surgery. The rate of index admission cholecystectomy improved over the study period (Figure 2). It remains unclear if IOC should be done routinely or selectively as part of the cholecystectomy. Gallstone pancreatitis falls into the category of “intermediate risk” (history of pancreatitis/jaundice, multiple small gallstones or elevated preoperative bilirubin, or ALKP levels) and therefore has been considered an indication to perform IOC in those countries performing selective IOC. Intraoperative cholangiogram in this context serves to identify filling defects which may require further intervention in the form of ERCP or bile duct exploration, and to identify any variations in anatomy that may complicate dissection and result in bile duct injury requiring repair.^9-11 False positive results may be due to air bubbles or failure of contrast to drain into duodenum due to another pathology such as papillary stenosis or periampullary edema due to pancreatitis.^9,14 In addition, one third of patients with true positive findings of CBD stones will pass the stone spontaneously within 6 weeks of surgery.^3,6,14,15 The true positive IOC rate in our study was 10% which is consistent with other studies which have shown incidence of choledocholithiasis on IOC at 12%.¹⁶

Routine IOC is associated with increased costs and operating room time, with a failure rate of 15%, and a false positive rate of 2-16% with some studies citing rates up to 60%, placing patients undergoing postoperative ERCP or bile duct exploration at potentially unnecessary risk of complications including post-ERCP pancreatitis, bleeding, duodenal perforation, or bile duct injury.^6,7,14,17 The failure rate in our study was 6% with a false positive rate of 7.4%. One of the reasons for the false positive rate might be the incorrect interpretation of the IOC which can be argued may be higher in those who perform IOC infrequently.

Our study showed the rate of choledocholithiasis was lower in those patients with normalizing preoperative bilirubin, while GGT, ALT, WCC, and CRP were not significant positive predictive factors; however, patients with worsening bilirubin levels were 2.93 times more likely to have a positive IOC than patients with normalizing bilirubin levels. Additionally, only 46.7% of patients who had a positive IOC went on to have a stone retrieved at the time of ERCP, indicating that 53.3% of patients were exposed to a potentially unnecessary medical procedure with its own associated risk, either through false positive IOC or the stone passing prior to intervention.^18,19 This is higher than other reports which show that only up to one third of patients with an abnormal IOC have a positive ERCP, and that patients at institutions with routine use of IOC had a 10-fold increased risk of undergoing postoperative ERCP.^{1, 20-22} There has also been a previously reported 5 fold increased risk of pancreatitis following ERCP after laparoscopic cholecystectomy compared to when done preoperatively.²³

The incidence of silent (non-jaundiced patient, non-dilated ducts) retained common bile duct stones is around 4% and only up to 15% of these will go on to become symptomatic.^1,9 It has been shown that most retained stones in the common bile duct are clinically non-significant or result in only minor and temporary symptoms, with only 5% of patients having a recurrent episode of pancreatitis requiring readmission.^1,7,11 Therefore, it has been proposed that on this basis, IOC use does not have a statistically significant effect on the rate of readmission for recurrent pancreatitis.¹ In patients who had a preoperative ERCP, only 18% (2 of 11 patients) had positive IOC with and only one patient needed postoperative ERCP.

Another factor to consider is the increased operative times associated with IOC which has been reported to add on average 10-28 minutes to the procedure which is consistent with our study where patients with a positive IOC outcome were 2 times more likely to have an increase in operation length, therefore increasing theater cost and resource consumption.^{1,10,17,18,24}

Pre-operative imaging with ultrasound or MRCP could also be considered before performing routine IOC. MRCP is considered to be the gold standard diagnostic test for patients with an intermediate probability of CBD stones (sensitivity 81-100% and specificity 92-100%) as ultrasound detection of biliary dilatation is 55-91%; however, MRCP can often be a difficult resource to access depending on the facility. With increasing availability and access to MRCP, it has been used to confirm choledocholithiasis prior to ERCP. In general, a CBD diameter of greater than 6 mm on ultrasound was found to be associated with a higher prevalence of choledocholithiasis, with detection of CBD stones in 23-80%, depending on body habitus and sonographer expertise and this modality is used more commonly.^9,16,19,20 However, our study demonstrated no association between CBD diameter on imaging and ERCP or IOC outcomes.

There were multiple limitations noted in this study. It is a retrospective study and therefore inherently biased. Additionally, there were significant changes to practice with regards to index admission operations for pancreatitis patients over the last 10 to 15 years, with recommendations now being that the operations are done at the index admission when data suggests that the majority here were discharged and operated on either in the private system or at a later time. This has decreased the number of patient records available to review. Operative and IOC techniques were not standardized between surgeons and therefore differences in operative lengths may be subject to confounders, and surgeon experience may play a role in the number of false positive intraoperative cholangiogram numbers; however, this is true reflection of real-world practice. Laparoscopic bile duct exploration is not routinely performed at our institution due to surgeon experience. It was also noted that there was no standardization of length of time between when the blood tests were taken. Length of stay was significantly variable between patients relating to length of time recovering from the initial pancreatitis and then awaiting ERCP and/or surgical intervention.

A recent systematic and meta-analysis of early vs delayed cholecystectomy for acute biliary pancreatitis showed definite advantages of early cholecystectomy on reducing recurrent pancreatitis and LOS²⁵; however, index admission cholecystectomy following mild acute biliary pancreatitis is still not routine practice despite various guidelines advocating index admission cholecystectomy. Reasons for a delayed cholecystectomy include resource availability, patient preference, and surgeon preference.^26,27

Intraoperative cholangiogram in patients with mild biliary pancreatitis is associated with a significant false positive IOC rate with majority of patients proceeding to an ERCP having no choledocholithiasis. A rising preoperative bilirubin is a predictor of a positive IOC and patients with normalizing bilirubin levels or a preoperative ERCP are less likely to have choledocholithiasis. These features may be used to select patients that would benefit from an IOC for index admission cholecystectomy following acute mild biliary pancreatitis.

Supplemental Material

Supplemental Material - Is Routine Intraoperative Cholangiogram Necessary in Patients With Mild Acute Biliary Pancreatitis Undergoing Index Admission Cholecystectomy?

Supplemental Material for Is Routine Intraoperative Cholangiogram Necessary in Patients With Mild Acute Biliary Pancreatitis Undergoing Index Admission Cholecystectomy? by Natalie M Quarmby, Minh Tu Vo, and Sivakumar Gananadha in The American Surgeon™.

Footnotes

Author Contributions

NQ undertook the acquisition, analysis and interpretation of the data along with drafting the work. MTV undertook analysis and interpretation of the data and SG conceptualized the project, interpreted the data, and substantially revised the work prior to submission. All authors have approved the submitted version and agree to be personally accountable for their own contributions and to ensure that questions related to the accuracy or integrity of any part of the work, even ones in which the author was not personally involved, are appropriately investigated, resolved, and the resolution documented in the literature.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Statement

ORCID iD

Natalie M. Quarmby

Data Availability Statement

All data used and/or analyzed during the current study are available from the corresponding author on reasonable request.*

Supplemental Material

Supplemental material for this article is available online.

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Supplementary Material

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