Risk factors for pancreatitis after pancreatic sphincterotomy: a review of 572 cases

• Introduction
• Patients and methods
• Technique
• Results
• Indications for EPS
• Technical aspects of EPS
• Discussion
• Acknowledgments
• References

Background and study aims: Endoscopic pancreatic sphincterotomy is indispensable for many therapeutic endoscopic maneuvers, but is also associated with a higher risk of pancreatitis after endoscopic retrograde cholangiopancreatography (ERCP). In this study, this subgroup of patients was investigated in order to identify risk factors and protective factors.
Patients and methods: A retrospective chart review identified 572 endoscopic pancreatic sphincterotomies that met the inclusion criteria. Charts were examined for indications, endoscopic technique, and outcomes, including pancreatitis.
Results: A total of 477 patients underwent 572 endoscopic pancreatic sphincterotomies during a 5-year period. Indications for sphincterotomy included chronic pancreatitis (n = 398), access for tissue sampling (n = 52), acute recurrent pancreatitis (n = 45), transpapillary drainage of a pancreatic pseudocyst (n = 32), precut access to the common bile duct (n = 29), and others (n = 16). Pancreatic duct drainage was performed in 69.1 % of the procedures (nasopancreatic catheter, n = 290, or pancreatic stent placement, n = 105). Post-ERCP pancreatitis occurred in 69 cases (12.1 %) and was severe in 10. The multivariate analysis identified female sex as being associated with a higher risk of pancreatitis, while an elevated C-reactive protein level, pancreatic ductal stones, sphincterotomy at only the major papilla, and pancreatic duct drainage with a nasopancreatic catheter or stent were associated with a lower risk.
Conclusions: This large series of patients undergoing endoscopic pancreatic sphincterotomy provides further evidence that both patient characteristics and technical factors modify the risk profile for post-ERCP pancreatitis. In addition to providing further definition of which patients are at risk, it also suggests that pancreatic duct drainage is an independently significant protective maneuver.

Introduction

Despite numerous technical advances in endoscopic retrograde cholangiopancreatography (ERCP), post-ERCP pancreatitis continues to be an important concern for endoscopists and patients. Numerous studies have helped define populations at increased risk of post-ERCP pancreatitis [1] [2] [3] [4] [5]. Although these studies have helped clarify which patients are at higher risk and encourage appropriate patient selection for ERCP, there is still a need for preventive strategies in the group of patients who are at higher risk. Not surprisingly, numerous strategies have been studied, including chemoprophylaxis, technique modifications, and temporary pancreatic drainage. The most promising of these is temporary pancreatic drainage, which has been studied mainly with small-diameter pancreatic stents [6] [7] [8] [9] [10], the majority of which migrate spontaneously. A recent meta-analysis [11] suggests that this treatment is effective in preventing post-ERCP pancreatitis, and it has been increasingly adopted by endoscopists as a preventive strategy.

Endoscopic pancreatic sphincterotomy (EPS) is often the first step in accessing the pancreatic duct for therapeutic maneuvers such as pancreatic duct stricture dilation, pancreatic duct stone removal, transpapillary pseudocyst drainage, and therapeutic pancreatic duct stent placement. It is also used by some expert endoscopists as a precut method for cannulating the biliary duct [12] [13]. While essential for most of these indications, pancreatic sphincterotomy has been shown in several studies to be an independent risk factor for post-ERCP pancreatitis [1] [2] [3] [4] [14]. Despite this, there is no information about specific risk factors within this subgroup of patients. Several studies of EPS have reported variable rates of main pancreatic duct (MPD) drainage and either have not assessed its effect on post-ERCP pancreatitis [12] [13] [15] [16] [17] [18] [19] [20], or have had very small numbers of patients without MPD drainage [21]. In addition, most of these studies involve fairly homogeneous patient populations, such as those with chronic pancreatitis or patients with difficult-to-cannulate biliary ducts. This type of study serves well for describing the technique and its complications in specific subgroups, but does not allow a more general evaluation of the properties of EPS and its complications. The present study was undertaken to review experience at a tertiary-care referral center with expertise in ERCP, and aims to identify risk factors for post-ERCP pancreatitis in patients undergoing EPS.

Patients and methods

All patients undergoing endoscopic pancreatic sphincterotomy in our center during a 5-year period (January 1999 - 31 December 2003) were identified through a review of a procedure log containing a record of all therapeutic biliary and pancreatic endoscopy procedures. Charts were then reviewed for further information, including the indications for the procedure - both for ERCP and for EPS - details of the procedure itself, and outcomes. The data were checked a second time for completeness in every patient by one of the authors (L. H.). The ethics committee of Erasmus University Hospital approved the study. Patients undergoing papillectomy for ampullomas and those with insufficient post-ERCP information were excluded. The latter group included those who were discharged on the same day as the procedure, so that retrospective evaluation of pain and/or blood chemistry 24 h after the ERCP was not possible in these cases. Although most of the patients underwent blood tests on the day after the procedure, some did not (33 %), usually because they were free of pain and were discharged that day. These patients were still included in the general analysis, but were not included in the assessment of post-sphincterotomy hyperamylasemia and hyperlipasemia. Preprocedure laboratory results were recorded within the 48 h before the EPS. The indications were classified firstly relative to the underlying reason for the ERCP - either pancreatic (stones, pseudocyst, ductal stenosis, malignancy, intrapapillary mucinous tumor) or biliary (stones, stricture, malignancy, sphincter of Oddi dysfunction, cholangitis, or other reasons); and secondly relative to the indication for the EPS itself (chronic pancreatitis, acute recurrent pancreatitis, access to the common bile duct to obtain tissue for diagnosis, for pancreatography, or for transpapillary drainage of a pancreatic pseudocyst following acute pancreatitis).

Technique

Before EPS, the duct is deeply cannulated and a guide wire is placed to anchor the sphincterotome and ensure access to the duct after sphincterotomy. A standard traction sphincterotome or a mini-tome (Wilson-Cook Medical, Inc., Winston-Salem, North Carolina, USA) is then used to carry out the EPS with pure cutting current, using an Erbe electrosurgical generator (Erbe Benelux BVBA, Diegem, Belgium). For pancreatic indications, the cut is directed between the 12-o’clock and 1-o’clock positions, whereas when it is used as a precut biliary access technique, the cut is directed more towards the biliary sphincter, toward the 11-o’clock position, with a length of 5 - 8 mm.

Post-ERCP pancreatitis was defined as new or worsened abdominal pain in combination with serum amylase or lipase 24 h raised after ERCP to more than three times the upper limit of normal (ULN), requiring an extended hospital stay of at least 48 h, as previously described [2] [22]. Pain was assessed by reviewing the medical and nursing notes. In patients in whom the preprocedure amylase and/or lipase levels were already elevated, the criteria were modified to include an increase of 50 % in amylase or lipase levels relative to the preprocedure levels. In accordance with the Atlanta Symposium and Cotton et al. criteria [22] [23], severe pancreatitis was defined as pancreatitis with organ failure and/or complications requiring an extended hospital stay. The procedure-related mortality was assessed at the end of the hospitalization period unless further follow-up was available.

Statistical analysis. Baseline and subgroup comparisons were carried out using Pearson’s chi-squared test for categorical data and the Mann-Whitney test for continuous data with a non-normal distribution. Factors that were found to be significant in the univariate analysis were entered into a stepwise logistic regression model to produce adjusted odds ratios (ORs). For the purpose of the multivariate analysis, both stent drainage and nasopancreatic catheter (NPC) drainage of the pancreatic duct were grouped into a single category as pancreatic duct drainage. The Hosmer-Lemeshow goodness-of-fit test was used to assess the calibration of the models, with a P value < 0.05 signifying a poor fit and a non-representative model.

Results

Six hundred pancreatic sphincterotomies were carried out during the 5-year study period. Twenty-eight patients were excluded from the analysis due to an inability to assess pain 24 h after the procedure (usually due to same-day discharge). Forty-five patients underwent more than one ERCP for pancreatic sphincterotomy, including five patients who underwent the procedure three times each. Thirty of these repeat procedures were pancreatic sphincterotomies of the same papilla (re-cut), while the remaining 15 were sphincterotomies of the other papilla. A total of 572 pancreatic sphincterotomies were therefore carried out in the 477 patients included in the analysis. The patients’ median age was 51 (interquartile range 42.5 - 63), and 357 of the sphincterotomies (62.4 %) were carried out in male patients.

Indications for EPS

A total of 398 sphincterotomies were carried out in patients with chronic pancreatitis; the baseline details are listed in Table [1]. The median duration of chronic pancreatitis prior to EPS was 3 years (IQR 1 - 7). The etiology of chronic pancreatitis included alcohol (n = 277, 69.6 %), idiopathic (n = 110, 27.6 %), and hereditary (n = 11, 2.8 %) causes. The majority of the patients (93.5 %) were suffering from chronic pancreatitis that was classified as moderate or severe at the time of sphincterotomy in accordance with the Cremer [24] and Cambridge [25] systems.

In all, 45 EPS procedures were carried out for recurrent acute pancreatitis. The median duration of disease in this group was 1.1 years (IQR 1.00 - 2.75), and the median number of attacks before EPS was three (IQR 3 - 6). The proportion of patients who were considered to have had severe recurrent pancreatitis was 37.8 %. In addition to pancreatitis, either chronic or recurrent acute, EPS procedures were carried out for other indications such as obtaining brush cytology/biopsies of suspected malignancy (n = 52), drainage of post-acute pancreatitis pseudocysts (n = 32), precut access to the biliary tract (n = 29), and other indications (n = 16).

Technical aspects of EPS

Endoscopic pancreatic sphincterotomy was carried out only at the major papilla in 452 of the procedures (79 %), only at the minor papilla in 90 (15.7 %), and at both papillae during the same procedure in 30 instances (5.2 %). EPS was performed on a previously untreated pancreatic sphincter in 477 cases (83.4 %) and was a re-cut procedure in the remaining 95 (16.6 %). Dilation of a pancreatic duct stricture was carried out in 169 of the cases and was performed with hydrostatic MaxForce balloon catheters with a diameter of 4 - 6 mm (Microvasive, Boston Scientific, Natick, Massachusetts, USA; n = 129), graduated Teflon bougies (Wilson-Cook; n = 30), or Soehendra stent extractors (Wilson-Cook; n = 10). Pancreatic duct cleaning with a balloon extraction catheter or stone basket extractor was performed during 178 of the procedures (31.1 %). Pancreatic duct drainage was conducted in 395 of the procedures (69.1 %), and consisted of NPC placement in 290 procedures and stenting in 105 (Figures [1], [2]). The vast majority (94.3 %) of the pancreatic duct stents were placed for periods longer than 1 week as a therapeutic measure rather than for purely prophylactic reasons. The duration of NPC drainage was a median of 2 days (IQR 1 - 3). In the group without pancreatic duct drainage (n = 177), 30 patients did not undergo drainage due to failure to achieve deep cannulation of the pancreatic duct, most often due to a stricture or intraductal stone, while 147 did not have drains placed at the endoscopist’s discretion. Concomitant biliary interventions included biliary sphincterotomy (n = 187) and bile duct stenting (n = 76).

When the groups were classified as those with chronic pancreatitis (n = 398), recurrent acute pancreatitis (n = 45), and other indications (n = 129), significant differences were observed in the prevalence of previously untreated pancreatic papillae, the distribution of sphincterotomies with respect to the major and minor papillae, and further therapeutic interventions, including pancreatic duct stricture dilations and duct cleaning. The drainage strategy was different as well, with a higher proportion of patients with chronic pancreatitis having drainage either by stent placement or NPC (Table [2]).

Post-ERCP pancreatitis occurred in 69 of the patients (12.1 %). Ten of these cases of pancreatitis were considered severe (indications for EPS: chronic pancreatitis, n = 4; acute recurrent pancreatitis, n = 2; common bile duct access, n = 2; intraductal papillary mucinous tumor, n = 1; and transpapillary pseudocyst drainage, n = 1). Most of these patients (seven of the 10) met the definition of severe pancreatitis solely on the basis of an extended hospital stay of more than 10 days, while two developed pseudocysts related to the pancreatitis. One 70-year-old man with mild chronic pancreatitis developed post-ERCP pancreatitis, which was complicated by acute respiratory distress syndrome and acute renal insufficiency. He was transferred to the intensive-care unit, but his condition continued to deteriorate and he died 2 weeks after ERCP. New or worsened postprocedural pain was present in 173 cases (30.2 %). Hyperamylasemia and/or hyperlipasemia occurred in 142 patients (including those with pain and hence overt pancreatitis), or in 36.8 % of the patients evaluated (with laboratory tests 24 - 48 h after ERCP). The median hospital stay duration was 3 days (IQR 2 - 5), and was significantly longer in patients who developed post-ERCP pancreatitis than in those who did not - 5 days (IQR 4 - 9) vs. 2 days (IQR 1 - 5; P < 0.0001).

The univariate analysis of potential risk factors identified female sex, recurrent acute pancreatitis, precut EPS for access to the common bile duct, intraductal papillary mucinous tumor, and EPS of only the minor papilla as being associated with a higher rate of post-ERCP pancreatitis (Table [3]). Factors significantly associated with a lower rate included chronic pancreatitis, a preprocedural C-reactive protein (CRP) level > 2 × ULN, the presence of pancreatic ductal stones, EPS of only the major papilla, dilation of pancreatic ductal stricture, pancreatic duct cleaning, and pancreatic duct drainage (Table [3]). When these factors were assessed in the multivariate analysis, female sex was associated with a higher risk of pancreatitis (OR 2.19; 95 % CI, 1.24 - 3.86), while preprocedure CRP > 2 × ULN (OR 0.37; 95 % CI, 0.18 - 0.76), pancreatic ductal stones (OR 0.42; 95 % CI, 0.22 - 0.81), pancreatic sphincterotomy of only the major papilla (OR 0.36; 95 % CI, 0.19 - 0.67), and pancreatic duct drainage (OR 0.47; 95 % CI, 0.26 - 0.85) were associated with a lower risk of pancreatitis (Table [4]).

Other complications, excluding pancreatitis, occurred in 23 cases (4 %). Significant post-sphincterotomy bleeding, defined as requiring further interventions such as transfusion or subsequent endoscopy, occurred in three patients (0.5 %), all of whom were discharged after treatment without further problems. Sepsis or cholangitis developed in 11 patients and was treated by antibiotics, with or without biliary drainage where appropriate. Retroperitoneal perforation occurred in five cases. Three of these perforations were recognized during the initial ERCP as a result of extravasation of contrast. These patients all had NPCs placed. The two remaining patients developed abdominal pain 6 - 10 h after the ERCP, and subsequent abdominal imaging revealed free retroperitoneal air. One of these patients underwent a second ERCP with placement of a nasobiliary catheter, while the other was treated conservatively with antibiotics and did well. All of the patients with retroperitoneal perforation/leakage were kept nil per os and received broad-spectrum intravenous antibiotics. Four of the five patients did well and were discharged a median of 14 days after ERCP. The fifth patient, a 79-year-old man, died of sepsis, renal failure, and congestive heart failure, but the death was 2 weeks after the ERCP, several days after the perforation had spontaneously sealed and without any obvious sequelae from it on subsequent computed tomography. Four patients in total died during the same hospitalization as the EPS procedure, including the patient with a retroperitoneal perforation just described and another with post-ERCP pancreatitis, described above. The other two patients who died were: a 79-year-old man with cholangiocarcinoma who developed deteriorating sepsis and multiple-organ failure and died 2 weeks after the ERCP; and a 69-year-old man with small-bowel adenocarcinoma who developed acute respiratory distress shortly after ERCP and died 2 weeks later of a pulmonary embolism.

Discussion

This study represents the largest series of patients undergoing pancreatic sphincterotomy published to date. Although these patients are known to be at higher risk of post-ERCP pancreatitis, this review has identified several factors that appear to be protective, as well as factors that place patients within this group at even higher risk. This information can be used by endoscopists to guide prophylactic therapy. Several studies have concluded that patient characteristics are as important, if not more so, than procedure-related factors [1] [2] [4] [5], and Freeman et al. have reported that these factors can be additive in relation to the risk [2]. As in previous studies, female sex was associated with a greater risk of post-ERCP pancreatitis in the present patient population, although the etiology behind this difference remains unknown. This study reinforces the point that even in a relatively high-risk population (patients undergoing EPS), there are characteristics of the patients that modify the risk profile.

Pancreatic duct drainage by insertion of an NPC or stent was associated with a significantly lower rate of pancreatitis. This strategy is based on the theory that the mechanism of post-ERCP pancreatitis is ductal hypertension resulting from edema after EPS [26] [27]. Further evidence to support this hypothesis may be the increased incidence of post-ERCP pancreatitis observed when EPS was performed on the minor papilla, which may be at higher risk of occlusion due the smaller size of the papilla and the fact that the pancreatic drainage is limited to one canal. Nasopancreatic catheters were placed more frequently than stents in this series (50.7 % vs. 18.7 % of cases, respectively). The advantages of these catheters in comparison with stents include the ability to remove them after 24 - 48 h without an additional endoscopy and the fact that they allow assessment of the need for therapeutic stent placement in patients with chronic pancreatitis - as pain with perfusion of saline and little or no drainage under fluoroscopic control after contrast injection are criteria for more permanent drainage.

The lower incidence of post-ERCP pancreatitis associated with a higher than normal CRP level is an interesting finding. This might perhaps again be related to patient selection or characteristics, as patients who have no current inflammation or infection - i. e. those most likely to have a normal CRP level - are at higher risk of post-ERCP pancreatitis. The corollary may be that carrying out EPS in a patient with ongoing inflammation, such as a flare of chronic pancreatitis, could be a relatively safe procedure. However, further research is needed to explore this finding.

Other studies have described series of patients undergoing EPS [15] [17] [18] [19] [21] but have all been much smaller than the current report, so that multivariate assessment was not possible. Precut EPS for biliary access was found to be a significant risk factor in the univariate analysis in the present study, but not in the multivariate analysis. Two other studies have also evaluated this technique in large groups of patients as well. Akashi et al. [12] describe a group of 172 patients who had biliary-access EPS performed, but do not mention the proportion of patients, if any, who underwent pancreatic duct drainage via stenting or NPC at the end of the procedure. They report a post-ERCP pancreatitis rate of 5.8 %, with none of the cases being severe. Kahaleh et al. [13] describe precut EPS for biliary access in 116 patients, only 25 % of whom had prophylactic pancreatic duct stents placed. Eight percent of the patients developed post-ERCP pancreatitis, with none of the cases being severe, and the authors observed a higher proportion of pancreatitis in the groups with pancreatic stents placed, although the difference did not reach statistical significance. Although these studies are interesting, comparisons with the present study are difficult due to the variable approaches to drainage used, different reporting methods, population differences, and even the definition of post-ERCP pancreatitis.

In conclusion, this study represents the largest series of patients undergoing EPS published to date. In fact, it may the last opportunity to examine the effect of pancreatic duct drainage on post-ERCP pancreatitis, as there is now a consensus that most patients who are at high risk of developing this complication, including those undergoing EPS, should receive temporary pancreatic duct drainage. The multivariate analysis confirms that patient characteristics are important determinants of the risk of post-ERCP pancreatitis, but that this risk appears to be reduced through pancreatic duct drainage, either temporary or prolonged. Whether the duration or type (NPC vs. small stents) of pancreatic duct drainage influences the risk factor is an area for future research.

Acknowledgments

L. C. Hookey, M.D. is supported by the Canadian Association of Gastroenterology/Canadian Institutes of Health Research/Solvay Research Fellowship Award.

The authors are grateful to N. Eleftheriadis, M.D., who helped with data collection and A. Vandermeeren, M.D. and P. Eisendrath, M.D., who participated in the management of the patients.

Competing interests: None declared.

References

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J. Devière, M.D., Ph. D.

Dept. of Gastroenterology · Erasmus University Hospital

Route de Lennik 808 · 1070 Brussels · Belgium

Fax: +32-2-555 4697

Email: jdeviere@ulb.ac.be

References

• 1 Aronson N, Flamm C R, Bohn R L. et al . Evidence-based assessment: patient, procedure, or operator factors associated with ERCP complications.  Gastrointest Endosc. 2002;  56 (6 Suppl) S294-S302
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  CrossrefPubMedSearch in Google Scholar
• 4 Masci E, Mariani A, Curioni S, Testoni P A. Risk factors for pancreatitis following endoscopic retrograde cholangiopancreatography: a meta-analysis.  Endoscopy. 2003;  35 830-834
  Thieme ConnectPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
• 6 Aizawa T, Ueno N. Stent placement in the pancreatic duct prevents pancreatitis after endoscopic sphincter dilation for removal of bile duct stones.  Gastrointest Endosc. 2001;  54 209-213
  CrossrefPubMedSearch in Google Scholar
• 7 Fazel A, Quadri A, Catalano M F. et al . Does a pancreatic duct stent prevent post-ERCP pancreatitis? A prospective randomized study.  Gastrointest Endosc. 2003;  57 291-294
  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  PubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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  Thieme ConnectPubMedSearch in Google Scholar
• 13 Kahaleh M, Tokar J, Mullick T. et al . Prospective evaluation of pancreatic sphincterotomy as a precut technique for biliary cannulation.  Clin Gastroenterol Hepatol. 2004;  2 971-977
  CrossrefPubMedSearch in Google Scholar
• 14 Devière J, Le Moine O, Van Laethem J L. et al . Interleukin 10 reduces the incidence of pancreatitis after therapeutic endoscopic retrograde cholangiopancreatography.  Gastroenterology. 2001;  120 498-505
  CrossrefPubMedSearch in Google Scholar
• 15 Ell C, Rabenstein T, Schneider H T. et al . Safety and efficacy of pancreatic sphincterotomy in chronic pancreatitis.  Gastrointest Endosc. 1998;  48 244-249
  PubMedSearch in Google Scholar
• 16 Heyries L, Barthet M, Delvasto C. et al . Long-term results of endoscopic management of pancreas divisum with recurrent acute pancreatitis.  Gastrointest Endosc. 2002;  55 376-381
  CrossrefPubMedSearch in Google Scholar
• 17 Jakobs R, Benz C, Leonhardt A. et al . Pancreatic endoscopic sphincterotomy in patients with chronic pancreatitis: a single-center experience in 171 consecutive patients.  Endoscopy. 2002;  34 551-554
  Thieme ConnectPubMedSearch in Google Scholar
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  CrossrefPubMedSearch in Google Scholar
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J. Devière, M.D., Ph. D.

Dept. of Gastroenterology · Erasmus University Hospital

Route de Lennik 808 · 1070 Brussels · Belgium

Fax: +32-2-555 4697

Email: jdeviere@ulb.ac.be