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Changing pattern of indications of endoscopic retrograde cholangiopancreatography in children and adolescents: a twelve-year experience 
Changing pattern of indications of endoscopic retrograde cholangiopancreatography in children and adolescents: a twelve-year experience
  Carlos O Kieling, Cristiane Hallal, Camila O Spessato, Luciana M Ribeiro, Helenice Breyer, Helena AS Goldani, Ismael Maguilnik
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Changing pattern of indications of endoscopic retrograde cholangiopancreatography in children and adolescents: a twelve-year experience
Carlos O Kieling, Cristiane Hallal, Camila O Spessato, Luciana M Ribeiro, Helenice Breyer, Helena AS Goldani, Ismael Maguilnik
Porto Alegre-RS, Brazil
Author Affiliations: Post-Graduate Program of Sciences in Gastro-enterology and Hepatology, Universidade Federal do Rio Grande do Sul (Kieling CO, Hallal C, Goldani HAS); Pediatric Gastroenterology Unit, Hospital de Cl¨ªnicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Brazil (Kieling CO, Hallal C, Spessato CO, Ribeiro LM, Goldani HAS); Endoscopy Service, Hospital de Cl¨ªnicas de Porto Alegre, Faculdade de Medicina, Universidade Federal do Rio Grande do Sul, Brazil (Breyer H, Maguilnik I)
Corresponding Author: Cristiane Hallal, Rua Ramiro Barcelos 2350, Porto Alegre-RS 90035-903, Brazil (Tel: 55-51-33597859; Fax: 55-51-33597859; Email: cris.hallal@yahoo.com)
Background: There are few data regarding endoscopic retrograde cholangiopancreatography (ERCP) usefulness in children and adolescents. We reviewed the long-term experience with diagnostic and therapeutic ERCP in a tertiary single center in Southern Brazil.
Methods: A retrospective chart review of patients aged 0-18 years who had undergone ERCPs from January 2000 to June 2012 was done. Data on demographics, indications, diagnosis, treatments, and complications were collected.
Results: Seventy-five ERCPs were performed in 60 patients. The median age of the patients at the procedure was 13.9 years (range: 1.2-17.9). Of the 60 patients, 47 (78.3%) were girls. Of all ERCPs, 48 (64.0%) were performed in patients above 10 years and 35 (72.9%) of them were in girls. ERCP was indicated for patients with bile duct obstruction (49.3%), sclerosing cholangitis (18.7%), post-surgery complication (12%), biliary stent (10.7%), choledochal cyst (5.3%), and pancreatitis (4%). The complication rate of ERCP was 9.7% involving mild bleeding, pancreatitis and cholangitis. Patients who had therapeutic procedures were older (13.7¡À3.9 vs. 9.9¡À4.9 years; P=0.001) and had more extrahepatic biliary abnormalities (82% vs. 50%; P=0.015) than those who had diagnostic ERCPs. A marked change in the indications of ERCPs was found, i.e., from 2001 to 2004, indications were more diagnostic and from 2005 therapeutic procedures were predominant.
Conclusions: Diagnostic ERCPs are being replaced by magnetic resonance cholangiopancreatography and also by endoscopic ultrasound. All these procedures are complementary and ERCP still has a role for therapeutic purposes.
                                                    World J Pediatr 2015;11(2):154-159
Key words: adolescents;
                    endoscopic retrograde
Endoscopic retrograde cholangiopancreatography (ERCP) is a recognized tool for the diagnosis and management of pancreatobiliary diseases.[1] ERCP guidelines have been well established in adults[2] but not for the pediatric population since its use is limited due to the low prevalence of pancreatobiliary diseases in this age group, technical and equipment limitations despite the advent of new duodenoscopes appropriate for the pediatric age, and the paucity of data regarding formal indications and safety.[3,4] The prevalence of different types of biliary and pancreatic diseases varies worldwide and, as a consequence, indications of ERCP may change in particular geographic areas.[5] Data regarding the utility and safety of ERCP in the pediatric population are limited to small sample sizes of patients.[6,7]
Given the lack of evidence-based guidelines for the use of ERCPs in children, this study aimed to review the 12-year experience with ERCPs in a single referral center in Southern Brazil in order to assess its usefulness and safety.
Study design
This study was approved by the Research Ethics Committee of Hospital de Cl¨ªnicas de Porto Alegre.From January 2000 to June 2012, the medical charts and ERCP reports of all patients under 18 years who had undergone ERCP were retrospectively reviewed from a specific hospital database and there were no missing data regarding patients who underwent ERCP. Data were collected regarding demographics, indications for the procedure, preoperative and final diagnosis, anesthesia type, success rate, treatment performed, and complications.
Indications were defined as therapeutic when a pancreaticobiliary disease treatable by ERCP was suspected based on clinical symptoms. Such treatments might be biliary sphincterotomy, bile duct stone extraction, biliary stricture dilation, biliary endoprosthesis, nasobiliary drainage tube placement, and bile duct orifice dilation. Diagnostic indication of ERCP was defined as the procedure when a pancreaticobiliary disease was suspected with no probable further therapeutic intervention.
All ERCP procedures were performed at Endoscopic Unit, Hospital de Cl¨ªnicas de Porto Alegre, a tertiary referral center for adult and pediatric gastroenterology and endoscopy. All procedures were performed by two well-trained endoscopists (BH and MI).
Procedures were performed in the Radiology Service and additional procedures such as stone extraction or stent placement were performed under radiological guidance. The ionic contrast Telebrix® 30 Meglumina (Guerbet Ltda, Rio de Janeiro, RJ) was used to opacify the pancreaticobiliary ducts. Obliteration of the intrahepatic biliary duct was defined by the absence of opacification of peripheral intrahepatic branches after injection of contrast under pressure.
Employed endoscope was the "diagnostic" duodenoscope (JF-100 Olympus America Corp., Melville, N.Y.), which has an outer diameter of 11.5 mm and an accessory channel diameter of 3.2 mm with a "therapeutic" duodenoscope (TJF-140; Olympus), with an outer diameter of 12.5 mm and accessory channel diameter of 4.2 mm.
Type of anesthesia was based on patient's age, anticipated patient collaboration, and pre-procedure diagnosis. Medications used were propofol alone or combined with midazolam and/or fentanyl and general anesthesia. All patients were assisted by an anesthesiologist following the American Society of Anesthesiologists classification as the hospital standard guidelines. All patients had cardiorespiratory monitoring by pulse oximeter and electrocardiogram assessment. No prophylactic antibiotics were used as it was not a local routine procedure.
Definition of complications
Following ERCP, the clinical status of children and liver and pancreatic function tests were monitored during the week after the procedure. Oral diet was initiated on the same day if the child did not complain of abdominal pain and if there was no significant increase in pancreatic enzymes 6 hours after the procedure. Success of the procedure was defined by the cannulation of the ampulla with biliary duct and/or pancreatic duct imaging. Failure of the procedure was defined as failure of cannulation after 6 attempts.
Pancreatitis was defined as the occurrence of abdominal pain associated with serum levels of amylase and lipase three times higher than normal values according to the age 24 hours or more after ERCP. Other ERCP-related complications were defined and graded in severity according to the consensus criteria developed by Cotton et al.[8,9]
Statistical analysis
Data were presented as mean¡ÀSD. Statistical analysis was performed by using the chi-square test, Fisher's Exact test, and Student's t test. Significance level was considered when P<0.05. Statistical analysis was performed using SPSS software version 18.
Over the 12-year study period, 75 ERCPs were performed in 60 patients from 1 to 18 years of age at our institution. The median age of the patients at the procedure was 13.9 years (range: 1.2-17.9). In this series, 47 ERCPs (62.7%) were performed in girls and 48 ERCPs (64.0%) in patients above 10 years. In patients aged 1 to 10 years, gender was equally distributed, but in those above 10 years ERCPs were performed more frequently in girls (72.9%) than in boys (Fig. 1).
The indications of ERCPs are shown in Table 1. ERCPs were indicated diagnostically for 32% of the patients but therapeutically for 68%. Two patients underwent ERCP because of acute pancreatitis suggested by the presence of Ascaris lumbricoides in the pancreaticobiliary duct shown by abdominal ultrasound.
Fifty-one patients had a single procedure, whereas 9 patients underwent more than one intervention (5 patients had 2 ERCPs, 2 had 3 ERCPs, and 2 had 4 ERCPs). The patients who underwent several ERCPs had post-surgery biliary complications such as post-liver transplantation biliary stenosis and post-cholecystectomy leak. The mean number of procedures per year was 6 (range: 4-13).
With regard to the type of sedation, 30 (40%) procedures were performed under general anesthesia and 45 (60%) under sedation and topical anesthesia of the pharynx with xylocaine spray. Variable doses of intravenous fentanyl and/or midazolam for conscious sedation and propofol for deep sedation were used.
The ampulla was cannulated and the procedure was successfully completed in 71 (94.7%) procedures. Four failures of cannulation were seen in 3 patients (2 patients had one failure each and another patient had 2 failures after 2 ERCP procedures).
ERCPs results are shown in Table 2. Fifty-five therapeutic procedures were performed (papilla sphincterotomy in 31 patients, stone extraction in 13, removal/replacement of biliary stent in 10, and removal of Ascaris lumbricoides in 1).
Five patients had mild acute pancreatitis, 1 had mild cholangitis and 1 had mild papilla bleeding. The overall complication rate was 9.3% (7/75). All of the patients were treated conservatively in less than 7 days with antibiotics and adrenalin, respectively. There was no mortality. Increased serum amylase and lipase after ERCPs were seen in 32 patients. Of these patients, 19 (59.4%) had increased rates 3 times higher than normal values, but all patients were asymptomatic. No pancreatic duct stents were placed for prophylaxis of post-ERCP pancreatitis.
Most of the patients aged above 10 years were girls (72.9% vs. 27.1%, P=0.024). Similarly, girls had diagnostic procedures rather than therapeutic ones (83.3% vs. 16.7%, P=0.012). With regard to abnormalities found on ERCP, there was no significant difference between boys and girls (P>0.05).
The patients who had therapeutic procedures were older (13.7¡À3.9 vs. 9.9¡À4.9 years, P=0.001) and had more extrahepatic biliary abnormalities (82% vs. 50%, P=0.015) than those who had diagnostic ERCPs. Intra-hepatic abnormalities were observed more frequently in diagnostic ERCPs than in therapeutic ones (45% vs. 16.7%, P=0.026).
There was a marked change in indications for ERCPs over the period of 2000-2012. In the first years, from 2001 to 2004, indications were more diagnostic, whereas from 2005 onwards therapeutic procedures were predominant, and since 2007 no more diagnostic indications were followed in our service (Fig. 2).
This study described a single center experience with ERCPs in a population aged from 1 to 18 years. This study highlighted the changes in indications for ERCP in the new era following the advent of imaging techniques, such as magnetic resonance cholangiopancreatography (MRCP) and endoscopic ultrasound (EUS).[10-12]
This is the first study in this age group from Southern Brazil. The indications for ERCP in our patients (choledocholithiasis and acute pancreatitis) were according to those described for Western adults[2] and children.[13,14] On the other hand, different indications were seen in Asian and Mediterranean countries that have a high prevalence of sickle cell disease and thus a high incidence of cholelithiasis and choledocholithiasis.[15-17] Choledochal cyst was the most frequent indication in Japan, India and Korea.[3,6,18] Recently, a large Western series has shown chronic or recurrent pancreatitis as the most common indication for ERCP and gallstone disease was an indication for only 26% of all ERCPs.[19] This might reflect the finding that gallstones in prepubertal children are rare as the patients of that study were younger than ours.
Differently from other studies in similar age groups, the second commonest indication for ERPC in our study was the investigation of biliary cirrhosis/sclerosing cholangitis. This might be due to the local characteristics of the Pediatric Unit as it is a referral center for liver diseases and liver transplantation; even though these indications have a decreasing trend as ERCPs are currently being gradually replaced by MRCPs in this group of patients.[20,21] Some studies have described more non-liver disease-related indications for ERCP such as chronic or acute pancreatitis, choledochal cyst and choledocholithiasis.[6,7,19,22,23] Another study has shown 84% of biliary indications and the majority of patients were younger than 1 year.[24]
In this study, the majority of patients above 10 years were girls and they had more diagnostic than therapeutic procedures. With regard to abnormalities found on ERCP, there was no significant difference between boys and girls, apart from gallstone disease which was higher in girls. These findings may be a reflex of the high risk of gallstone disease in females, especially from the fertile years onwards as this may be related to the female sex hormones.[25]
In this study, ERCP was successfully performed in 94.7% of the patients, which is in accordance with that in a similar age group ranging from 89.5% to 97.5%.[6,12,22,26-28] Some factors may impair the success of the cannulation of the ampulla with biliary duct and/or pancreatic duct imaging such as anatomical abnormalities, previous surgery and inadequate sedation.[29,30] Nonetheless, successful cannulation rates at or above 95% are consistently achieved by experienced endoscopists.[30,31]
The complication rate after ERCP was reported to range from 3.4% to 28.5% in children and pancreatitis was the most common cause.[6,14,22,24-27,32,33] In our study, the complication rate was 10% and acute pancreatitis was the most common minor complication, which is similar to the rate in adults (10%).[34-36] This finding indicates the skills and experience of the endoscopists. The complication rate is lower in adult ERCPs performed by endoscopists who perform 100 ERCPs than by those who perform 40 ERCPs per year.[37] We believe that the pancreatitis rate post-ERCP in our study would have been lower if some prophylactic strategies had been employed. In adults, pancreatic stent has been recommended for patients at high risk and periprocedural rectal administration of nonsteroidal anti-inflammatory drugs for low-risk patients with post-ERCP pancreatitis.[38,39] However, these prophylactic strategies were not used in our series.
In the past decades, new diagnostic modalities for pancreatobiliary disorders have been developed, including MRCP and EUS in adults and children.[11,12] MRCP seems to be an alternative to ERCP in the assessment of various entities such as choledochal cyst, recurrent pancreatitis, primary sclerosing cholangitis, and post-liver transplantation biliary stenosis.[7,40-45] As in other centers,[32] ERCPs in our service are being replaced by MRCPs for diagnostic purpose since 2004 following the development of MRCPs. Nevertheless, ERCP is still considered important as a therapeutic procedure for gallstone diseases.[1] In our study, therapeutic procedures accounted for 73.3% of all ERCPs, of which 67.3% were indicated for biliary obstruction.
There were several limitations in this study. This study was a retrospective review, and many data regarding long-term follow up to assess later complications of the procedures were missed. However, we found that patients who underwent therapeutic ERCPs were older and had more extrahepatic biliary abnormalities than those who had diagnostic ERCPs. The patients who had diagnostic ERCPs had intra-hepatic abnormalities.
In conclusion, ERCP is a useful and safe procedure for children and adolescents with a complication rate similar to that seen in adults. Diagnostic ERCPs are being replaced by MRCPs and EUSs, but ERCPs are still used for therapeutic purposes.
Funding: This study was funded by FIPE - Hospital de Clinicas de Porto Alegre.
Ethical approval: This study was approved by the Research Ethics Committee of Hospital de Clinicas de Porto Alegre.
Competing interest: All authors declare no conflict of interest.
Contributors: KCO was responsible for the research design and data analysis. HC, SCO and RLM collected the data. GHAS analyzed the data and wrote the manuscript. BH and MI performed the ERCP procedures. All authors read and approved the final version of the manuscript.
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                                          Received February 21, 2014  Accepted after revision July 22, 2014
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