Post-ERCP pancreatitis in 2364 ERCP procedures: is intraductal ultrasonography another risk factor?

• Introduction
• Patients and methods
• Data collection
• Exclusions
• Definition of post-ERCP pancreatitis
• Statistical analysis
• Results
• Procedures
• Post-ERCP pancreatitis
• Clinical outcome
• Univariate analysis
• Multivariate analysis
• Discussion
• References

Background and study aims: Acute pancreatitis is considered a relevant major complication following endoscopic retrograde cholangiopancreatography (ERCP); according to literature data, the incidence varies between 1.5 % and 17 %. In the present study, we aimed to identify potentially new, hitherto unknown risk factors for post-ERCP pancreatitis.

Patients and methods: A total of 2364 ERCP procedures performed in 1275 patients during the years 2004 – 2008 were included in the study. Post-ERCP pancreatitis was defined as acute abdominal pain within 48 hours following ERCP with at least 3-fold elevated levels of serum lipase and a requirement for analgesic drugs for at least 24 hours. The severity of the pancreatitis was determined using the Imrie score.

Results: In our cohort study a total of 54 different patients (2.3 %) developed post-ERCP pancreatitis. In 50 of these patients (92.6 %) the pancreatitis was mild; in 54 (7.4 %) it was severe. Patients with post-ERCP pancreatitis had highly significantly lower bilirubin levels than patients who did not have post-ERCP pancreatitis (P < 0.001). Length of hospital stay, duration of analgesics, and need for analgesic drugs were significantly higher in patients suffering from severe pancreatitis (P ≤ 0.01). In multivariate analysis, among other, already well-described risk factors we identified intraductal ultrasonography as another risk factor for post-ERCP pancreatitis, with a hazard ratio of 2.41 (P = 0.004).

Conclusions: According to our retrospective data, intraductal ultrasonography seems to be another independent risk factor for developing post-ERCP pancreatitis, which needs to be further elucidated in prospective studies.

Introduction

The pathogenesis of pancreatitis occurring after endoscopic retrograde cholangiopancreatography (ERCP) is assumed to be multifactorial, and includes a combination of chemical, hydrostatic, enzymatic, mechanical, and thermal factors [1]. A number of risk factors acting independently or in combination have been identified. These include investigator-related factors, patient-related factors, and method-related factors [2]. Numerous studies have analyzed endoscopic and pharmacologic interventions to reduce the risk of post-ERCP pancreatitis [3], with conflicting results. Due to the development of noninvasive imaging procedures such as magnetic resonance cholangiopancreatography (MRCP) and endoscopic ultrasonography (EUS), the need for ERCP as a diagnostic procedure is declining. For therapeutic use, however, pathology, intraductal tumor staging with intraductal ultrasonography, or cholangioscopic ERCP remains the gold standard [4] [5] [6]. For this reason, the need to reduce the risk of post-ERCP pancreatitis remains.

Acute pancreatitis is one of the major complications occurring after ERCP [7]. The majority of attacks are mild and self-limiting, but up to 15 % are severe with potentially life-threatening complications [8] [9]. Elevated serum levels of lipase are common after the ERCP procedure, occurring in up to 70 % of patients [10]. The diagnosis of acute clinical pancreatitis requires a set of symptoms including abdominal pain, a need for analgesics, and hyperlipasemia.

ERCP accounts for the majority of cases of iatrogenic acute pancreatitis. The incidence of post-ERCP pancreatitis varies and depends on the selection of patients and the endoscopist’s experience [11] [12] [13]. The most common scoring systems assessing the severity of acute pancreatitis are the APACHE-2, Ranson, and Imrie systems [14] [15]. In the present study we retrospectively confirmed and identified various risk factors for the development of post-ERCP pancreatitis so as to be able to set the right indication for this procedure.

Relating to the identification of potential risk factors for post-ERCP pancreatitis after insertion of catheter-like probes (e. g., biopsy forceps) [1] [2], we were interested whether intraductal ultrasonography might act as a hitherto unknown risk factor.

Patients and methods

We retrospectively analyzed the data relating to our patients at Münster University Hospital who underwent ERCP in the years 2004 – 2008. A total of 1275 patients were enrolled in the study, in whom a total of 2364 ERCPs had been performed. We analyzed all the patient charts together with the stored serum lipase measurements obtained between 4 and 24 hours after the ERCP procedure had been performed. The names of all patients who had undergone ERCP during the study period were identified by searching for Code K85 (International Classification of Diseases, ICD). This ensured that all patients with post-ERCP pancreatitis were included.

Standard ERCP cannulation was performed using a 7-Fr catheter with a tapered tip (Fluoro TIP catheter; Boston Scientific, Natick, Massachusetts, USA). The catheter was inserted directly into the orifice of the common bile duct. If smooth sliding into the common bile duct was not possible, precut sphincterotomy was performed followed by conventional sphincterotomy over a guide wire (Metro 25 wire, 480 cm length; Cook Medical, Bloomington, Indiana, USA).

Data collection

The clinical records of patients with post-ERCP hyperlipasemia were collected. The indication for ERCP and its diagnostic or therapeutic purpose as well as the nature of ERCP-related interventions were recorded. Information regarding postprocedural symptoms and clinical findings supporting the diagnosis of acute pancreatitis, duration of abdominal pain, need for analgesia and its duration, need for intravenous hydration and its duration, time of resumption of oral diet, procedure-related complications, and postprocedural hospital stay was retrieved. In addition, postprocedural Imrie scores at 24 and 48 hours were calculated.

Exclusions

Patients who underwent ERCP for acute biliary pancreatitis, patients with a history of post-ERCP pancreatitis, and patients with prior sphincterotomy were excluded, as their post-ERCP clinical course might not reflect the effect of ERCP-induced pancreatitis.

Definition of post-ERCP pancreatitis

The following definition of acute post-ERCP pancreatitis was used in this study ([Table 1]): The abdominal pain should persist for 24 hours.

Serum lipase has to be more than three times normal. (At Münster University Hospital, the normal range for serum lipase is taken to be 13 – 60 U/L). Using the Imrie scoring system, attacks were classified as mild if associated with minimal organ dysfunction and an uneventful recovery, while severe attacks were defined as those associated with an Imrie score above 2.

Statistical analysis

Data were analyzed using SPSS 16.0 (SPSS Inc., Chicago, Illinois, USA). Results are expressed as medians and ranges. Comparison between groups was performed using the Mann–Whitney U-test, the Wilcoxon U-test, and the χ² test as appropriate. A P-value below 0.05 was considered statistically significant. Univariate analysis for screening purposes for risk factors was performed using the odds ratio. In addition, multivariate analysis calculating the hazard ratio using logistic binary regression was added on the factors identified by univariate analysis as independently significant for post-ERCP pancreatitis. For multivariate analysis, to avoid bias only the first ERCP procedure was considered, as the probability of recurrent acute pancreatitis might be increased with each further ERCP procedure in patients who had already suffered from post-ERCP pancreatitis.

Results

Procedures

In our cohort study, 1275 patients had undergone 2364 ERCPs between 2004 and 2008. Patient demographics, indications, and interventions performed are outlined in [Table 2].

Subtracting interventional ERCP procedures including intraductal ultrasonography (IDUS) and transpapillary biopsies (in patients with unexplained biliary stenosis) from a total of 2364 ERCPs, a total of 531 purely diagnostic procedures remained (22.5 %). In about a third (35.8 %), ERCP was indicated for benign or malignant bile duct stenosis. In these cases, initial endoscopic access via ERCP was not possible (e. g., due to filiform stenosis of the common bile duct). Thirty-nine patients (7.3 %) suffered from choledocholithiasis with giant calculi where primary extraction seemed an unfavorable option and extracorporeal shockwave lithotripsy was preferred. Other indications for diagnostic ERCP included persistently elevated markers of cholestasis (37.6 %), cystic pancreatic lesions (10.8 %), primary biliary cholangitis (PBC) or primary sclerosing cholangitis (PSC) (4.8 %), and fever due to suspected cholangitis (3.6 %). No patients had ERCP for evaluation of suspected sphincter of Oddi dysfunction, so no biliary or pancreatic manometry was used. The interventions were performed by six independent investigators rated as highly experienced according to the generally accepted guidelines [16], with a case volume above 200/year.

Post-ERCP pancreatitis

A total of 613 patients developed hyperlipasemia (25.6 %) within 24 hours after ERCP procedure. A review of the clinical records of the patients with hyperlipasemia indicated that 54 independent events (2.3 %) fulfilled the definition of post-ERCP pancreatitis as outlined in [Table 1], 50 of which (92.6 %) were mild ERCP-induced attacks of acute pancreatitis and represented group A of the study. Four patients (7.4 %) developed severe post-ERCP pancreatitis (group B). The mean age of patients in group A, who were mainly male (79 %), was 57.4 (±16.2) years and did not differ statistically from the mean age in group B (62.3 ± 17.6 years). No statistical difference in terms of body mass index was noted between the two groups (24.2 vs. 22.3, P = 0.37). Of the 2364 ERCPs performed, 1833 (77.5 %) included interventions: endoscopic sphincterotomy (27 %), placement of self-expanding metal stent (3 %), plastic stent insertion (41 %), calculus extraction (16 %), IDUS (18 %), and transpapillary biopsy (16 %). Patients developing post-ERCP pancreatitis had highly significantly lower bilirubin levels than patients not suffering from post-ERCP pancreatitis (1.1 mg/dL vs. 3.8 mg/dL, P < 0.001).

Clinical outcome

As shown in [Table 3], patients with mild pancreatitis had a significantly shorter duration of abdominal pain (P = 0.002), required highly significantly lower doses of opiate analgesia (P<0.001), and received analgesics (opiate and nonopiate; P = 0.002) and intravenous hydration (P = 0.034) for significantly shorter periods of time than patients with severe pancreatitis.

Post-ERCP hospital stay was highly significantly shorter (P = 0.002) in group A. Diabetes mellitus does not seem to be a relevant risk factor for the severity of post-ERCP pancreatitis as a significant difference in terms of diabetes distribution was not observed. The elevation of serum lipase did not correlate significantly with the severity of pancreatitis (P = 0.55) ([Table 3]).

Univariate analysis

Subgroup analysis revealed differences in the way interventions were performed. In the post-ERCP pancreatitis group, significantly more sphincterotomies, transpapillary biopsies, and IDUS examinations were performed (P < 0.001). In univariate analysis, the odds ratio for developing post-ERCP pancreatitis was 3.33 (95 % confidence interval: 1.83 – 6.05) in patients receiving transpapillary biopsies, 2.46 (95 %CI 1.36 – 4.46) in patients undergoing IDUS, 2.39 (95 %CI 1.33 – 4.30) in patients with sphincterotomy, and 2.74 (95 %CI 1.04 – 7.21) in patients with a juxtapapillary diverticulum, while patients with choledocholithiasis did not have a higher odds ratio of developing post-ERCP pancreatitis. In 22 of 481 sphincterotomies the cutting direction was pancreatic and associated with a significantly higher risk for the development of post-ERCP pancreatitis ([Table 4]). Precut sphincterotomy turned out to be an additional risk factor (odds ratio 3.35).

The implantation of a plastic stent in the biliary tract did not show a protective benefit. On the other hand, implantation of pancreatic stents due to stenosis of the pancreatic duct, drainage of pancreas pseudocysts, or pancreatic calculi was associated with a significantly higher risk of post-ERCP pancreatitis, as presented in [Table 4]. Pancreatic stents were not implanted solely for prevention of post-ERCP pancreatitis, nor was pharmacological prophylaxis used. The odds ratio for developing post-ERCP pancreatitis was 3.64 (95 %CI 1.64 – 8.04) in patients with a serum bilirubin concentration below 1.5 mg/dL ([Table 4]).

Multivariate analysis

Multivariate analysis results for pancreatitis are shown in [Table 5].

Six factors were identified as independent risk factors for post-ERCP pancreatitis. The following interventions were at increased risk: IDUS (hazard ratio 2.41 [95 %CI 1.33 – 4.39]), transpapillary biopsy (HR 4.88 [95 %CI 2.6 – 9.15]), sphincterotomy (HR 2.35 [95 %CI 1.31 – 4.23]), juxtapapillary diverticulum (HR 2.75 [95 %CI 1.04 – 7.25]), serum bilirubin < 1.5 mg/dL (HR 3.77 [95 %CI 1.68 – 8.48]), and benign stenosis (HR 1.92 [95 %CI 1.05 – 3.49]). The presence of malignant stenosis (HR 0.23 [95 %CI 0.1 – 0.58]) and elevated serum bilirubin levels (HR 0.42 [95 %CI 0.22 – 0.83]) predicted significantly fewer complications ([Table 5]).

Applying the nonparametric Mann–Whitney and Wilcoxon U-tests, a tendency towards a higher risk of developing post-ERCP pancreatitis was seen in patients undergoing IDUS with EST, but it did not reach statistical significance (P = 0.051).

Discussion

In our patient cohort more than 70 % of all ERCP procedures were interventional; patient surveillance was ensured for at least 24 hours after ERCP. The 2.3 % rate of post-ERCP pancreatitis seems low in comparison with recent publications [17] [18]. Factors which have been associated with increased risk of post-ERCP pancreatitis include normal serum bilirubin, pre-existing pancreatitis, prior ERCP-induced pancreatitis, absence of chronic pancreatitis, sphincter of Oddi dysfunction, difficulty of cannulation, biliary sphincterotomy, failed clearing of biliary stones, and pancreatic endoscopic sphincterotomy [9] [11] [12] [19].

In our study, using univariate and multivariate analysis we were able to confirm procedure-related and patient-related risk factors for post-ERCP pancreatitis as shown in [Tables 4] and [5]. It is noteworthy that in our cohort study we were able to identify IDUS as another independent risk factor. Up to the present, this possibility has only been discussed by Matsubayashi and colleagues [20]: in their study, which included only 477 patients, post-ERCP pancreatitis was recognized in 9.6 % of subjects who had undergone ERCP-associated diagnostic examination using at least one additional diagnostic modality (biopsy, brush cytology, IDUS, peroral cholangioscopy or pancreatoscopy) with an odds ratio of 4.6 (P < 0.0001); however, no statistical significance was detected for IDUS when multivariate analysis was applied.

In our department, IDUS as valuable tool for diagnosis of biliary diseases such as suspected malignancy or unclear distal biliary duct stenosis [21] [22] [23] [24] [25] [26] [27] [28] [29] [30] was performed 418 times from 2004 to 2008. A total of 20 patients (only one patient with severe pancreatitis) developed acute pancreatitis after an ERCP procedure that involved biliary IDUS. For biliary IDUS, we used miniprobes alone, without wire guidance (6 Fr/15 MHz or Fr/20 MHz; Aloka Co. Ltd., Tokyo, Japan). In multivariate analysis, a hazard ratio of 2.41 (P = 0.004) was calculated. Mechanical irritation of the papilla with consequent swelling might be a feasible pathogenic mechanism. Possibly miscannulation of the pancreatic duct with the rigid, inflexible tip of the EUS miniprobe adds to the risk of post-ERCP pancreatitis. Potential miscannulations, however, were not recorded on our ERCP reports and could therefore not be investigated in our study. Mechanical irritation, such as by deep wire insertion of the pancreatic duct, has been shown to increase the risk of post-ERCP pancreatitis, as reported by Freeman et al. [11]. In particular, the usual combination of biliary IDUS with sphincterotomy or transpapillary biopsy further increases the risk of acute pancreatitis according to our statistical data analysis ([Table 4]). We observed a tendency (P = 0.051) towards a higher risk of developing post-ERCP pancreatitis in patients undergoing IDUS plus EST within the same endoscopic session.

It should be mentioned that the rate of severe pancreatitis in IDUS-ERCPs was considerably lower. This is of importance as we were able to demonstrate that patients with mild pancreatitis have significantly shorter hospital stays and less need of analgesic drugs ([Table 3]). In several studies, sensitivity, specificity, and accuracy rates of 84 % – 91 %, 80 % – 94 %, and 84 % – 90 %, respectively, were found for biliary IDUS, indicating the tremendous impact of IDUS in biliary system diagnostics [29] [30] [31]. So far, according to the literature, IDUS has not been considered as a potential risk factor in a larger cohort study. Since our results refer to a retrospective data analysis, this new, striking finding needs to be further investigated in a prospective manner. Considering the results of the present, retrospectively performed study revealing IDUS as potential risk factor for post-ERCP pancreatitis, the decision to employ IDUS should be take with care so long as no further prospective study exists that addresses this issue in detail. The use of biliary IDUS should therefore be restricted to high-volume centers with experienced personnel to guarantee low complication rates in terms of acute pancreatitis.

The generalizability of our findings is certainly open to question because all examinations were performed at a single tertiary referral center and data were collected retrospectively. A prospective multicenter study with a high case volume might further confirm our observations.

Our study shows that ERCP is a safe method that carries a low risk for the development of acute pancreatitis in a high-volume endoscopic center even if the vast majority of ERCPs are interventional. In our patient cohort the majority of affected patients develop self-limiting mild pancreatitis. We were able to confirm juxtapapillary diverticulum, serum bilirubin concentration below 1.5 mg/dL, sphincterotomy, and transpapillary biopsy (n = 2 – 5) as independent risk factors for post-ERCP pancreatitis.

Interestingly, IDUS was found to be an independent risk factor for post-ERCP pancreatitis with a hazard ratio of 2.41 (P = 0.004). This observation in a high-volume center with a considerably lower risk for post-ERCP pancreatitis has not been described before. Nevertheless, IDUS itself has revolutionized the diagnosis of intraductal pathologies and remains an important tool in the diagnosis of pancreaticobiliary diseases [21] [22] [23] [24] [25] [26] [28] [29]. Because of the significant higher risk of post-ERCP pancreatitis, however, the authors suggest that the use of IDUS should be restricted to well-defined indications and high-volume centers with particularly experienced endoscopists.

Competing interests: None

References

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1 The first two authors, T. Meister and H. Heinzow, contributed equally to this work.

D. DomagkMD 

Department of Medicine B
University of Münster

Albert-Schweitzer-Str. 33
48149 Münster
Germany

Fax: +49-251-8347576

Email: domagkd@uni-muenster.de

References

• 1 Sherman S. ERCP and endoscopic sphincterotomy-induced pancreatitis.  Am J Gastroenterol. 1994;  89 303-305
  PubMedSearch in Google Scholar
• 2 Freeman M L, Overby C, Qi D. Pancreatic stent insertion: consequences of failure and results of a modified technique to maximize success.  Gastrointest Endosc. 2004;  59 8-14
  CrossrefPubMedSearch in Google Scholar
• 3 Testoni P A. Simple measures to prevent post-ERCP pancreatitis?.  Gut. 2008;  57 1197-1198
  CrossrefPubMedSearch in Google Scholar
• 4 Fujita N, Noda Y, Kobayashi G et al. Endoscopic approach to early diagnosis of pancreatic cancer.  Pancreas. 2004;  28 279-281
  CrossrefPubMedSearch in Google Scholar
• 5 Hawes R H. Diagnostic and therapeutic uses of ERCP in pancreatic and biliary tract malignancies.  Gastrointest Endosc. 2002;  56 (6 Suppl) S201-S205
  CrossrefPubMedSearch in Google Scholar
• 6 Fukuda Y, Tsuyuguchi T, Sakai Y et al. Diagnostic utility of peroral cholangioscopy for various bile-duct lesions.  Gastrointest Endosc. 2005;  62 374-382
  CrossrefPubMedSearch in Google Scholar
• 7 Cotton P B, Lehman G, Vennes J et al. Endoscopic sphincterotomy complications and their management: an attempt at consensus.  Gastrointest Endosc. 1991;  37 383-393
  CrossrefPubMedSearch in Google Scholar
• 8 Cheng C L, Sherman S, Watkins J L et al. Risk factors for post-ERCP pancreatitis: a prospective multicenter study.  Am J Gastroenterol. 2006;  101 139-147
  CrossrefPubMedSearch in Google Scholar
• 9 Freeman M L, Nelson D B, Sherman S et al. Complications of endoscopic biliary sphincterotomy.  N Engl J Med. 1996;  335 909-918
  CrossrefPubMedSearch in Google Scholar
• 10 Pieper-Bigelow C, Strocchi A, Levitt M D. Where does serum amylase come from and where does it go?.  Gastroenterol Clin North Am. 1990;  19 793-810
  PubMedSearch in Google Scholar
• 11 Freeman M L, DiSario J A, Nelson D B et al. Risk factors for post-ERCP pancreatitis: a prospective, multicenter study.  Gastrointest Endosc. 2001;  54 425-434
  CrossrefPubMedSearch in Google Scholar
• 12 Loperfido S, Angelini G, Benedetti G et al. Major early complications from diagnostic and therapeutic ERCP: a prospective multicenter study.  Gastrointest Endosc. 1998;  48 1-10
  CrossrefPubMedSearch in Google Scholar
• 13 Williams E J, Taylor S, Fairclough P et al. Risk factors for complication following ERCP; results of a large-scale, prospective multicenter study.  Endoscopy. 2007;  39 793-801
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  CrossrefPubMedSearch in Google Scholar
• 15 Knaus W A, Draper E A, Wagner D P et al. APACHE II: a severity of disease classification system.  Crit Care Med. 1985;  13 818-829
  CrossrefPubMedSearch in Google Scholar
• 16 Faigel D, Baron T, Lewis B et al. Ensuring competence in endoscopy. Prepared by the ASGE Taskforce on Ensuring Competence in Endoscopy and American College of Gastroenterology Executive and Practice Management Committees. ASGE policy and procedures manual for gastrointestinal endoscopy: guidelines for training and practice on CD-ROM. 2005: 1-36
  Search in Google Scholar
• 17 Cotton P B, Garrow D A, Gallagher J et al. Risk factors for complications after ERCP: a multivariate analysis of 11,497 procedures over 12 years.  Gastrointest Endosc. 2009;  70 80-88
  CrossrefPubMedSearch in Google Scholar
• 18 Bailey A A, Bourke M J, Williams S J et al. A prospective randomized trial of cannulation technique in ERCP: effects on technical success and post-ERCP pancreatitis.  Endoscopy. 2008;  40 296-301
  Thieme ConnectPubMedSearch in Google Scholar
• 19 Vandervoort J, Soetikno R M, Tham T C et al. Risk factors for complications after performance of ERCP.  Gastrointest Endosc. 2002;  56 652-656
  CrossrefPubMedSearch in Google Scholar
• 20 Matsubayashi H, Fukutomi A, Kanemoto H et al. Risk of pancreatitis after endoscopic retrograde cholangiopancreatography and endoscopic biliary drainage.  HPB (Oxford). 2009;  11 222-228
  CrossrefPubMedSearch in Google Scholar
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1 The first two authors, T. Meister and H. Heinzow, contributed equally to this work.

D. DomagkMD 

Department of Medicine B
University of Münster

Albert-Schweitzer-Str. 33
48149 Münster
Germany

Fax: +49-251-8347576

Email: domagkd@uni-muenster.de