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Cho E, Kim SH, Park CH, Yoon JH, Lee SO, Kim TH, Chon HK. Tailored Hydration With Lactated Ringer's Solution for Postendoscopic Retrograde Cholangiopancreatography Pancreatitis Prevention: A Randomized Controlled Trial. Am J Gastroenterol 2024; 119:2426-2435. [PMID: 38912692 DOI: 10.14309/ajg.0000000000002903] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/04/2024] [Accepted: 06/06/2024] [Indexed: 06/25/2024]
Abstract
INTRODUCTION Aggressive hydration using lactated Ringer's solution prevents postendoscopic retrograde cholangiopancreatography (ERCP) pancreatitis (PEP). Concerns of this strategy are large volume and lengthy hydration. Our study aimed to evaluate the efficacy of tailored aggressive hydration (TAH) for PEP prevention. METHODS In this prospective, multicenter, double-blinded, randomized trial conducted across 3 tertiary Korean hospitals, patients who underwent ERCP for the first time were randomly assigned (1:1) to the tailored standard hydration (TSH) and TAH groups. The TSH group received 1.5 mL/kg/hr lactated Ringer's solution during and after ERCP, whereas the TAH group was administered a 20 mL/kg bolus post-ERCP and 3 mL/kg/hr during and after the procedure. Both groups were assessed for elevated serum amylase levels and pain 4-6 hours after ERCP. If both were absent, hydration was discontinued. If either was present, hydration was continued at the original rate until 8 hours. The primary end point was PEP development and was analyzed on an intention-to-treat analysis. RESULTS A total of 344 patients were randomly assigned to treatment groups (171 to the TSH group and 172 to the TAH group). PEP was observed in 9.4% (16/171) in the TSH group and 3.5% (6/172) in the TAH group (relative risk 0.37, 95% confidence interval 0.15-0.93, P = 0.03). No difference was identified between the 2 groups in PEP severity ( P = 0.80) and complications related to volume overload ( P = 0.32). DISCUSSION TAH according to the presence of abdominal pain or elevated serum amylase levels at 4-6 hours after ERCP is safe and prevents PEP development.
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Affiliation(s)
- Eunae Cho
- Division of Gastroenterology, Department of Internal Medicine, Chonnam National University Medical School, Chonnam National University Hospital, Gwangju, South Korea
| | - Seong-Hun Kim
- Division of Gastroenterology, Department of Internal Medicine, Jeonbuk National University Medical School and Research Institute of Clinical Medicine, Jeonbuk National University-Biomedical Research Institute, Jeonbuk National University Hospital, Jeonju, South Korea
| | - Chang Hwan Park
- Division of Gastroenterology, Department of Internal Medicine, Chonnam National University Medical School, Chonnam National University Hospital, Gwangju, South Korea
| | - Jae Hyun Yoon
- Division of Gastroenterology, Department of Internal Medicine, Chonnam National University Medical School, Chonnam National University Hospital, Gwangju, South Korea
| | - Seung Ok Lee
- Division of Gastroenterology, Department of Internal Medicine, Jeonbuk National University Medical School and Research Institute of Clinical Medicine, Jeonbuk National University-Biomedical Research Institute, Jeonbuk National University Hospital, Jeonju, South Korea
| | - Tae Hyeon Kim
- Division of Biliopancreatology, Department of Internal Medicine, Wonkwang University Hospital, Wonkwang University School of Medicine, Iksan, Korea
| | - Hyung Ku Chon
- Division of Biliopancreatology, Department of Internal Medicine, Wonkwang University Hospital, Wonkwang University School of Medicine, Iksan, Korea
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Rojas-Victoria EJ, Hernández-Ruiz SI, García-Perdomo HA. Effectiveness of the pharmacological therapy to prevent post ERCP acute pancreatitis: a network meta-analysis. Expert Rev Gastroenterol Hepatol 2024; 18:203-215. [PMID: 38725175 DOI: 10.1080/17474124.2024.2345640] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/02/2023] [Accepted: 04/17/2024] [Indexed: 05/24/2024]
Abstract
OBJECTIVE To determine the effectiveness of the different pharmacological agents in preventing post-ERCP acute pancreatitis. METHODS We included clinical trials of pharmacological interventions for prophylaxis of acute post-ERCP pancreatitis. The event evaluated was acute pancreatitis. We conducted a search strategy in MEDLINE (OVID), EMBASE, and Cochrane Central Register of Controlled Trials from inception to nowadays. We reported the information in terms of relative risks (RR) with a 95% confidence interval. We assessed the heterogeneity using the I2 test. RESULTS We included 84 studies for analysis (30,463 patients). The mean age was 59.3 years (SD ± 7.01). Heterogeneity between studies was low (I2 = 34.4%) with no inconsistencies (p = 0.2567). Post ERCP pancreatitis was less in prophylaxis with NSAIDs (RR 0.65 95% CI [0.52 to 0.80]), aggressive hydration with Lactate Ringer (RR 0.32 95% CI [0.12-0.86]), NSAIDs + isosorbide dinitrate (RR 0.28 95% CI [0.11-0.71]) and somatostatin and analogues (RR 0.54 [0.43 to 0.68]) compared with placebo. CONCLUSIONS NSAIDs, the Combination of NSAIDs + isosorbide dinitrate, somatostatin and analogues, and aggressive hydration with lactate ringer are pharmacological strategies that can prevent post-ERCP pancreatitis when compared to placebo. More clinical trials are required to determine the effectiveness of these drugs.
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Affiliation(s)
| | | | - Herney Andrés García-Perdomo
- Division of Urology/Urooncology, Department of Surgery, School of Medicine, Universidad del Valle, Cali, Colombia
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El Kurdi B, Imam Z, Abonofal A, Babar S, Shah P, Pannala R, Papachristou G, Echavarria J, Pisipati S, Jahangir S, Rajalingamgari P, Chang YHH, Singh VP. NSAIDs do not reduce severity among post-ERCP pancreatitis patients. Pancreatology 2024; 24:14-23. [PMID: 37981523 PMCID: PMC11298787 DOI: 10.1016/j.pan.2023.11.003] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/15/2023] [Revised: 10/05/2023] [Accepted: 11/01/2023] [Indexed: 11/21/2023]
Abstract
OBJECTIVE Non-steroidal anti-inflammatory drugs (NSAIDs) are the most studied chemoprophylaxis for post-endoscopic retrograde cholangiopancreatography pancreatitis (PEP). While previous systematic reviews have shown NSAIDs reduce PEP, their impact on moderate to severe PEP (MSPEP) is unclear. We conducted a systematic review and meta-analysis to understand the impact of NSAIDs on MSPEP among patients who developed PEP. We later surveyed physicians' understanding of that impact. DESIGN A systematic search for randomized trials using NSAIDs for PEP prevention was conducted. Pooled-prevalence and Odds-ratio of PEP, MSPEP were compared between treated vs. control groups. Analysis was performed using R software. Random-effects model was used for all variables. Physicians were surveyed via email before and after reviewing our results. RESULTS 7688 patients in 25 trials were included. PEP was significantly reduced to 0.598 (95%CI, 0.47-0.76) in the NSAIDs group. Overall burden of MSPEP was reduced among all patients undergoing ERCP: OR 0.59 (95%CI, 0.42-0.83). However, NSAIDs didn't affect the proportion of MSPEP among those who developed PEP (p = 0.658). Rectal Indomethacin and diclofenac reduced PEP but not MSPEP. Efficacy didn't vary by risk, timing of administration, or bias-risk. Survey revealed a change in the impression of the effect of NSAIDs on MSPEP after reviewing our results. CONCLUSIONS Rectal diclofenac or indomethacin before or after ERCP reduce the overall burden of MSPEP by reducing the pool of PEP from which it can arise. However, the proportion of MSPEP among patients who developed PEP is unaffected. Therefore, NSAIDs prevent initiation of PEP, but do not affect severity among those that develop PEP. Alternative modalities are needed to reduce MSPEP among patients who develop PEP.
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Affiliation(s)
- Bara El Kurdi
- Department of Internal Medicine East Tennessee State University, Johnson City, TN, USA; Division of Gastroenterology and Hepatology, University of Texas Health at San Antonio, TX, USA.
| | - Zaid Imam
- Division of Gastroenterology and Hepatology, William Beaumont Hospital, Royal Oak, MI, USA
| | - Abdulrahman Abonofal
- Department of Internal Medicine East Tennessee State University, Johnson City, TN, USA
| | - Sumbal Babar
- Department of Internal Medicine East Tennessee State University, Johnson City, TN, USA
| | - Pir Shah
- Division of Gastroenterology and Hepatology, University of Texas Health at San Antonio, TX, USA
| | - Rahul Pannala
- Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Georgios Papachristou
- Division of Gastroenterology and Hepatology, The Ohio State University Wexner Medical Center, Columbus, OH, USA
| | - Juan Echavarria
- Division of Gastroenterology and Hepatology, University of Texas Health at San Antonio, TX, USA
| | - Sailaja Pisipati
- Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Sarah Jahangir
- Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Prasad Rajalingamgari
- Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Yu-Hui H Chang
- Department of Biostatistics, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Vijay P Singh
- Division of Gastroenterology and Hepatology, Mayo Clinic Arizona, Scottsdale, AZ, USA.
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Akshintala VS, Kanthasamy K, Bhullar FA, Sperna Weiland CJ, Kamal A, Kochar B, Gurakar M, Ngamruengphong S, Kumbhari V, Brewer-Gutierrez OI, Kalloo AN, Khashab MA, van Geenen EJM, Singh VK. Incidence, severity, and mortality of post-ERCP pancreatitis: an updated systematic review and meta-analysis of 145 randomized controlled trials. Gastrointest Endosc 2023; 98:1-6.e12. [PMID: 37004815 DOI: 10.1016/j.gie.2023.03.023] [Citation(s) in RCA: 40] [Impact Index Per Article: 20.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/04/2021] [Revised: 03/01/2023] [Accepted: 03/21/2023] [Indexed: 04/04/2023]
Abstract
BACKGROUND AND AIMS The incidence, severity, and mortality of post-ERCP pancreatitis (PEP) largely remain unknown with changing trends in ERCP use, indication, and techniques. We sought to determine the incidence, severity, and mortality of PEP in consecutive and high-risk patients based on a systemic review and meta-analysis of patients in placebo and no-stent arms of randomized control trials (RCTs). METHODS The MEDLINE, Embase, and Cochrane databases were searched from the inception of each database to June 2022 to identify full-text RCTs evaluating PEP prophylaxes. The incidence, severity, and mortality of PEP from the placebo or no-stent arms of RCTs were recorded for consecutive and high-risk patients. A random-effects meta-analysis for a proportions model was used to calculate PEP incidence, severity, and mortality. RESULTS One hundred forty-five RCTs were found with 19,038 patients in the placebo or no-stent arms. The overall cumulative incidence of PEP was 10.2% (95% confidence interval [CI], 9.3-11.3), predominantly among the academic centers conducting such RCTs. The cumulative incidences of severe PEP and mortality were .5% (95% CI, .3-.7) and .2% (95% CI, .08-.3), respectively, across 91 RCTs with 14,441 patients. The cumulative incidences of PEP and severe PEP were 14.1% (95% CI, 11.5-17.2) and .8% (95% CI, .4-1.6), respectively, with a mortality rate of .2% (95% CI, 0-.3) across 35 RCTs with 3733 patients at high risk of PEP. The overall trend for the incidence of PEP among patients randomized to placebo or no-stent arms of RCTs has remained unchanged from 1977 to 2022 (P = .48). CONCLUSIONS The overall incidence of PEP is 10.2% but is 14.1% among high-risk patients based on this systematic review of placebo or no-stent arms of 145 RCTs; this rate has not changed between 1977 and 2022. Severe PEP and mortality from PEP are relatively uncommon.
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Affiliation(s)
- Venkata S Akshintala
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | - Kavin Kanthasamy
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | - Furqan A Bhullar
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | | | - Ayesha Kamal
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | - Bharati Kochar
- Division of Gastroenterology, Massachusetts General Hospital, Boston, Massachusetts, USA
| | - Merve Gurakar
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | | | - Vivek Kumbhari
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | | | - Anthony N Kalloo
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | - Mouen A Khashab
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
| | - Erwin-Jan M van Geenen
- Department of Gastroenterology and Hepatology, Radboud University Medical Center, Nijmegen, Netherlands
| | - Vikesh K Singh
- Division of Gastroenterology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
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Wu CCH, Lim SJM, Khor CJL. Endoscopic retrograde cholangiopancreatography-related complications: risk stratification, prevention, and management. Clin Endosc 2023; 56:433-445. [PMID: 37460103 PMCID: PMC10393565 DOI: 10.5946/ce.2023.013] [Citation(s) in RCA: 10] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/12/2022] [Accepted: 01/11/2023] [Indexed: 07/29/2023] Open
Abstract
Endoscopic retrograde cholangiopancreatography (ERCP) plays a crucial role in the management of pancreaticobiliary disorders. Although the ERCP technique has been refined over the past five decades, it remains one of the endoscopic procedures with the highest rate of complications. Risk factors for ERCP-related complications are broadly classified into patient-, procedure-, and operator-related risk factors. Although non-modifiable, patient-related risk factors allow for the closer monitoring and instatement of preventive measures. Post-ERCP pancreatitis is the most common complication of ERCP. Risk reduction strategies include intravenous hydration, rectal nonsteroidal anti-inflammatory drugs, and pancreatic stent placement in selected patients. Perforation is associated with significant morbidity and mortality, and prompt recognition and treatment of ERCP-related perforations are key to ensuring good clinical outcomes. Endoscopy plays an expanding role in the treatment of perforations. Specific management strategies depend on the location of the perforation and the patient's clinical status. The risk of post-ERCP bleeding can be attenuated by preprocedural optimization and adoption of intra-procedural techniques. Endoscopic measures are the mainstay of management for post-ERCP bleeding. Escalation to angioembolization or surgery may be required for refractory bleeding. Post-ERCP cholangitis can be reduced with antibiotic prophylaxis in high risk patients. Bile culture-directed therapy plays an important role in antimicrobial treatment.
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Affiliation(s)
- Clement Chun Ho Wu
- Department of Gastroenterology and Hepatology, Singapore General Hospital, Singapore
- Duke-NUS Medical School, Singapore
| | - Samuel Jun Ming Lim
- Department of Gastroenterology and Hepatology, Singapore General Hospital, Singapore
- Duke-NUS Medical School, Singapore
| | - Christopher Jen Lock Khor
- Department of Gastroenterology and Hepatology, Singapore General Hospital, Singapore
- Duke-NUS Medical School, Singapore
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Post-ERCP Pancreatitis: Prevention, Diagnosis and Management. Medicina (B Aires) 2022; 58:medicina58091261. [PMID: 36143938 PMCID: PMC9502657 DOI: 10.3390/medicina58091261] [Citation(s) in RCA: 28] [Impact Index Per Article: 9.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/08/2022] [Revised: 08/21/2022] [Accepted: 08/26/2022] [Indexed: 11/17/2022] Open
Abstract
Endoscopic retrograde cholangiopancreatography (ERCP) carries a post-ERCP pancreatitis (PEP) rate of 2–10%, which could be as high as 30–50% in high-risk cases. PEP is severe in up to 5% of cases, with potential for life-threatening complications, including multi-organ failure, peripancreatic fluid collections, and death in up to 1% of cases. The risk of PEP is potentially predictable and may be modified with pharmacological measures and endoscopist technique. This review covers the definition, epidemiology and risk factors for PEP, with a focus on the latest evidence-based medical and endoscopic strategies to prevent and manage PEP.
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Shi QQ, Huang GX, Li W, Yang JR, Ning XY. Rectal nonsteroidal anti-inflammatory drugs, glyceryl trinitrate, or combinations for prophylaxis of post-endoscopic retrograde cholangiopancreatography pancreatitis: A network meta-analysis. World J Clin Cases 2022; 10:7859-7871. [PMID: 36158503 PMCID: PMC9372852 DOI: 10.12998/wjcc.v10.i22.7859] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/10/2021] [Revised: 12/04/2021] [Accepted: 07/06/2022] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Acute pancreatitis is the most common and severe complication of endoscopic retrograde cholangiopancreatography (ERCP). Recent evidence suggests that combinations based on rectal nonsteroidal anti-inflammatory drugs (NSAIDs) are more beneficial in preventing post-ERCP pancreatitis (PEP). Randomized controlled trials (RCTs) have also demonstrated the efficacy of glyceryl trinitrate (GTN). We conducted a network meta-analysis to compare NSAIDs and GTN for prevention of PEP and to determine whether they are better in combination.
AIM To compare NSAIDs and GTN for prevention of PEP and to determine whether they are better in combination.
METHODS A systematic search was done for full-text RCTs of PEP in PubMed, Embase, Science Citation Index, and the Cochrane Controlled Trials database. Inclusion and exclusion criteria were used to screen for eligible RCTs. The major data were extracted by two independent reviewers. The frequentist model was used to conduct this network meta-analysis and obtain the pairwise OR and 95%CI. The data were then extracted and assessed on the basis of the Reference Citation Analysis (https://www.referencecitationanalysis.com/).
RESULTS Twenty-four eligible RCTs were selected, evaluating seven preventive strategies in 9416 patients. Rectal indomethacin 100 mg plus sublingual GTN (OR: 0.21, 95%CI: 0.09–0.50), rectal diclofenac 100 mg (0.34, 0.18–0.65), sublingual GTN (0.34, 0.12–0.97), and rectal indomethacin 100 mg (0.49, 0.33–0.73) were all more efficacious than placebo in preventing PEP. The combination of rectal indomethacin and sublingual GTN had the highest surface under the cumulative ranking curves (SUCRA) probability of (92.2%) and was the best preventive strategy for moderate-to-severe PEP with a SUCRA probability of (89.2%).
CONCLUSION Combination of rectal indomethacin 100 mg with sublingual GTN offered better prevention of PEP than when used alone and could alleviate the severity of PEP.
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Affiliation(s)
- Qing-Qing Shi
- Department of Health Management Center, The People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Guo-Xiu Huang
- Department of Health Management Center, The People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Wei Li
- Department of Health Management Center, The People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Jian-Rong Yang
- Department of Hepatobiliary, Pancreas and Spleen Surgery, The People's Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, Guangxi Zhuang Autonomous Region, China
| | - Xiao-Yi Ning
- Department of Hematology, The Frist People’s Hospital of Nanning, Nanning 530021, Guangxi Zhuang Autonomous Region, China
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Zhang Q, Deng DH, Liu J, Chen WW, Chen J, Chen CW. Application of non-steroidal anti-inflammatory drugs in prevention of pancreatitis after endoscopic retrograde cholangiopancreatography. Shijie Huaren Xiaohua Zazhi 2022; 30:198-203. [DOI: 10.11569/wcjd.v30.i4.198] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023] Open
Abstract
Endoscopic retrograde cholangiopancreatography (ERCP) is one of the most important methods for the clinical diagnosis and treatment of biliary and pancreatic diseases. Post-ERCP pancreatitis (PEP) is the most common complication. Non-steroidal anti-inflammatory drugs (NSAIDs) are commonly used in clinical prevention of PEP, but the application standards are not unified. This article reviews the progress in the research of the preventive effect of different types of NSAIDs on PEP, their administration routes, timing, and dosage, and combination with other drugs, as well as the preventive effect of NSAIDs in different risk stratification populations, and points out that indomethacin and diclofenac are the most commonly used types of NSAIDs, which should be given at 100 mg via rectal administration before ERCP in all non-selected patients with no contraindications.
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Affiliation(s)
- Qian Zhang
- Dalian Medical University, Dalian 116000, Liaoning Province, China
| | - Deng-Hao Deng
- Department of Gastroenterology, Subei People's Hospital of Jiangsu Province, Yangzhou 225001, Jiangsu Province, China
| | - Jun Liu
- Department of Gastroenterology, Subei People's Hospital of Jiangsu Province, Yangzhou 225001, Jiangsu Province, China
| | - Wei-Wei Chen
- Department of Gastroenterology, Subei People's Hospital of Jiangsu Province, Yangzhou 225001, Jiangsu Province, China
| | - Juan Chen
- Department of Gastroenterology, Subei People's Hospital of Jiangsu Province, Yangzhou 225001, Jiangsu Province, China
| | - Chao-Wu Chen
- Department of Gastroenterology, Subei People's Hospital of Jiangsu Province, Yangzhou 225001, Jiangsu Province, China
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Yu S, Shen X, Li L, Bi X, Chen P, Wu W. Rectal indomethacin and diclofenac are equally efficient in preventing pancreatitis following endoscopic retrograde cholangiopancreatography in average-risk patients. JGH Open 2021; 5:1119-1126. [PMID: 34621996 PMCID: PMC8485396 DOI: 10.1002/jgh3.12643] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/23/2021] [Accepted: 08/04/2021] [Indexed: 11/22/2022]
Abstract
Rectal indomethacin and diclofenac are promising drugs for prevention of post‐endoscopic retrograde cholangiopancreatography (ERCP) pancreatitis (PEP). However, their prophylactic effect on PEP in average‐risk patients remains controversial. We performed a systematic review and meta‐analysis to assess the efficacy and safety of rectal indomethacin and diclofenac in average‐risk patients, and to indirectly compare the prophylactic effect of the two drugs. A comprehensive search of the PubMed, EMBASE, and Cochrane Library databases was performed to identify randomized controlled trials (RCTs) on rectal indomethacin or diclofenac for prophylaxis against PEP. Fixed‐ and random‐effects models weighted by the Mantel–Haenszel method were used for direct comparisons. The adjusted indirect treatment comparison method was used to indirectly compare the efficacy of indomethacin and diclofenac. A total of 10 RCTs, including 2928 patients, met our inclusion criteria. No significant publication bias was identified. Pooled estimates showed that rectal indomethacin and diclofenac were associated with a significant reduction in the overall risk of PEP compared with control intervention [relative risk (RR) = 0.62; 95% confidence interval (CI): 0.46–0.83] in average‐risk patients. Subgroup analyses showed that both rectal indomethacin (RR = 0.67; 95% CI: 0.49–0.94) and diclofenac (RR = 0.42; 95% CI: 0.23–0.75) were effective in the prevention of PEP. Indirect comparison showed no significant difference between the effectiveness of the two drugs in the prevention of PEP (RR = 1.607; 95% CI: 0.824–3.136). The updated meta‐analysis suggests that both drugs provide equivalent protection against PEP in average‐risk patients.
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Affiliation(s)
- Shuang Yu
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
| | - Xumu Shen
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
| | - Liang Li
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
| | - Xiaofei Bi
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
| | - Ping Chen
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
| | - Wei Wu
- Department of Gastroenterology Chongqing University Three Gorges Hospital Chongqing China
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Ribeiro IB, do Monte Junior ES, Miranda Neto AA, Proença IM, de Moura DTH, Minata MK, Ide E, dos Santos MEL, Luz GDO, Matuguma SE, Cheng S, Baracat R, de Moura EGH. Pancreatitis after endoscopic retrograde cholangiopancreatography: A narrative review. World J Gastroenterol 2021; 27:2495-2506. [PMID: 34092971 PMCID: PMC8160616 DOI: 10.3748/wjg.v27.i20.2495] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/10/2020] [Revised: 01/30/2021] [Accepted: 03/18/2021] [Indexed: 02/06/2023] Open
Abstract
Acute post-endoscopic retrograde cholangiopancreatography pancreatitis (PEP) is a feared and potentially fatal complication that can be as high as up to 30% in high-risk patients. Pre-examination measures, during the examination and after the examination are the key to technical and clinical success with a decrease in adverse events. Several studies have debated on the subject, however, numerous topics remain controversial, such as the effectiveness of prophylactic medications and the amylase dosage time. This review was designed to provide an update on the current scientific evidence regarding PEP available in the literature.
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Affiliation(s)
- Igor Braga Ribeiro
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | | | - Antonio Afonso Miranda Neto
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | - Igor Mendonça Proença
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | | | - Mauricio Kazuyoshi Minata
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | - Edson Ide
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | | | - Gustavo de Oliveira Luz
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | - Sergio Eiji Matuguma
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | - Spencer Cheng
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
| | - Renato Baracat
- Department of Gastrointestinal Endoscopy Unit, University of São Paulo School of Medicine, São Paulo 05403-010, Brazil
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Bhatt H. Post-Endoscopic Retrograde Cholangiopancreatography Pancreatitis: An Updated Review of Current Preventive Strategies. Clin Exp Gastroenterol 2021; 14:27-32. [PMID: 33564256 PMCID: PMC7866941 DOI: 10.2147/ceg.s276361] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 08/19/2020] [Accepted: 01/13/2021] [Indexed: 12/11/2022] Open
Abstract
Pancreatitis is a serious complication of endoscopic retrograde cholangiopancreatography, with incidence rates as high as 16% in some centers. Recent studies have also shown an upward trend in hospitalization due to endoscopic retrograde cholangiopancreatography-related pancreatitis. Early interventions taken before, during, and after the procedure can significantly reduce the risk of pancreatitis and decrease morbidity and mortality of the patients. To select appropriate patients for endoscopic retrograde cholangiopancreatography, in-depth knowledge of the patient-related and procedure-related risk factors is required. This updated clinical review outlines various pharmacological agents and surgical methods used for the prevention of post-endoscopic retrograde cholangiopancreatography pancreatitis. Current evidence supports the use of rectal non-steroidal anti-inflammatory drugs and pancreatic stent placement as an effective preventive strategy. Further research is needed to compare these preventive modalities to improve patient outcomes after endoscopic retrograde cholangiopancreatography.
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Affiliation(s)
- Harshil Bhatt
- Goshen Hospital, Goshen, IN, USA
- Indiana University School of Medicine, South Bend, IN, USA
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Serrano JPR, Jukemura J, Romanini SG, Aguilar PFG, Castro JSLD, Torres IT, Pulla JAS, Neto OM, Taglieri E, Ardengh JC. Nonsteroidal anti-inflammatory drug effectivity in preventing post-endoscopic retrograde cholangiopancreatography pancreatitis: A systematic review and meta-analysis. World J Gastrointest Endosc 2020; 12:469-487. [PMID: 33269056 PMCID: PMC7677884 DOI: 10.4253/wjge.v12.i11.469] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/20/2020] [Revised: 06/24/2020] [Accepted: 09/18/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Endoscopic retrograde cholangiopancreatography (ERCP) is the primary therapeutic procedure for the treatment of diseases affecting the biliary tree and pancreatic duct. Although the therapeutic success rate of ERCP is high, the procedure can cause complications, such as acute pancreatitis [post-ERCP pancreatitis (PEP)], bleeding and perforation. AIM To assess the efficacy of non-steroidal anti-inflammatory drugs (NSAIDs) in preventing PEP during follow-up. METHODS Databases such as MEDLINE, EMBASE and Cochrane Central Library were searched. Only randomized controlled trials (RCTs) comparing the efficacy of NSAIDs and placebo for the prevention of PEP were included. Outcomes evaluated included the incidence of PEP, severity of pancreatitis, route of administration, types, dose, and timing of administration of NSAIDs. RESULTS Twenty-six RCTs were considered eligible with a total of 8143 patients analyzed. Overall, 4020 patients used NSAIDs before ERCP and 4123 did not use NSAIDs (control group). Ultimately, 298 cases of post-ERCP acute pancreatitis were diagnosed in the NSAID group and 484 cases in the placebo group. The risk of PEP was lower in the NSAID group risk difference (RD): -0.04; 95% confidence interval (CI): -0.07 to - 0.03; number needed to treat (NNT), 25; P < 0.05. NSAID use effectively prevented mild pancreatitis compared to placebo use (2.5% vs 4.1%; 95%CI: -0.05 to -0.01; NNT, 33; P < 0.05), but information on moderate PEP and severe PEP could not be fully elucidated. Only rectal administration reduced the incidence of PEP with RD: -0.06; 95%CI: -0.08 to -0.04; NNT, 17; P < 0.05). Furthermore, only the use of diclofenac or indomethacin was effective in preventing PEP, at a dose of 100 mg, which must be administered before performing ERCP. CONCLUSION Rectal administration of diclofenac and indomethacin significantly reduced the risk of developing mild PEP. Additional RCTs are needed to compare the efficacy between NSAID routes of administration in preventing PEP.
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Affiliation(s)
| | - José Jukemura
- Department of Gastroenterology, University of Sao Paulo, São Paulo 05403-000, São Paulo, Brazil
| | - Samuel Galante Romanini
- Department of Gastrointestinal Endoscopy Service, Hospital 9 de Julho, São Paulo 01409002, São Paulo, Brazil
| | | | | | - Isabela Trindade Torres
- Department of Gastrointestinal Endoscopy Service, Hospital 9 de Julho, São Paulo 01409002, São Paulo, Brazil
| | | | - Otavio Micelli Neto
- Department of Gastrointestinal Endoscopy Service, Hospital 9 de Julho, São Paulo 01409002, São Paulo, Brazil
| | - Eloy Taglieri
- Department of Gastrointestinal Endoscopy Service, Hospital 9 de Julho, São Paulo 01409002, São Paulo, Brazil
| | - José Celso Ardengh
- Department of Gastroenterology, University of Sao Paulo, São Paulo 05403-000, São Paulo, Brazil
- Department of Gastrointestinal Endoscopy Service, Hospital 9 de Julho, São Paulo 01409002, São Paulo, Brazil
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Ahmad W, Okam NA, Torrilus C, Rana D, Khatun MK, Jahan N. Pharmacological Prevention of Post-Endoscopic Retrograde Cholangiopancreatography Pancreatitis: Where Do We Stand Now? Cureus 2020; 12:e10115. [PMID: 33005532 PMCID: PMC7523742 DOI: 10.7759/cureus.10115] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022] Open
Abstract
Post-endoscopic retrograde cholangiopancreatography pancreatitis (PEP) is the most frequently occurring complication of endoscopic retrograde cholangiopancreatography (ERCP). PEP is associated with significant morbidity and mortality; that is why the prevention of PEP is essential. Pharmacoprevention holds a central position in PEP prophylaxis. The current literature explores the efficacy of various pharmacological agents in preventing PEP, their routes of administration, and the correct administration timing. Data was collected on PubMed using regular keywords, the latter yielded 2077 papers. After applying inclusion and exclusion criteria, 218 papers were selected and screened and 28 studies were finally chosen after the removal of duplicate and irrelevant studies. The selected 28 articles comprised 25 randomized clinical trials and three systematic reviews. The study concludes that rectal non-steroidal anti-inflammatory drugs (NSAIDs) administered before ERCP are effective in preventing PEP in high-risk patients. The efficacy of rectal NSAIDs in low to medium risk group is not well established. A combination of rectal NSAIDs and intravenous hydration provides improved prophylaxis against PEP in high-risk patients than NSAIDs alone. Nafamostat, sublingual nitrates, and intravenous hydration are potential alternatives in patients with contraindications to NSAIDs.
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Serrano JPR, de Moura DTH, Bernardo WM, Ribeiro IB, Franzini TP, de Moura ETH, Brunaldi VO, Salesse MT, Sakai P, De Moura EGH. Nonsteroidal anti-inflammatory drugs versus placebo for post-endoscopic retrograde cholangiopancreatography pancreatitis: a systematic review and meta-analysis. Endosc Int Open 2019; 7:E477-E486. [PMID: 30957004 PMCID: PMC6445649 DOI: 10.1055/a-0862-0215] [Citation(s) in RCA: 44] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/21/2018] [Accepted: 01/29/2019] [Indexed: 02/08/2023] Open
Abstract
Background and study aims Endoscopic retrograde cholangiopancreatography (ERCP) is the primary therapeutic procedure for treatment of diseases that affect the biliary tree and pancreatic duct. While the therapeutic success rate of ERCP is high, the procedure can cause complications, such as acute pancreatitis (PEP), bleeding, and perforation. This meta-analysis aimed to assess the efficacy of nonsteroidal anti-inflammatory drugs (NSAIDs) in preventing PEP following (ERCP). Materials and methods We searched databases, such as MEDLINE, Embase, and Cochrane Central Library. Only randomized controlled trials (RCTs) that compared the efficacy of NSAIDs and placebo for the prevention of PEP were included. Outcomes assessed included incidence of PEP, severity of pancreatitis, route of administration, and type of NSAIDs. Results Twenty-one RCTs were considered eligible with a total of 6854 patients analyzed. Overall, 3427 patients used NSAIDs before ERCP and 3427 did not use the drugs (control group). In the end, 250 cases of acute pancreatitis post-ERCP were diagnosed in the NSAIDs group and 407 cases in the placebo group. Risk for PEP was lower in the NSAID group (risk difference (RD): -0.05; 95 % confidence interval (CI): -0.07 to - 0.03; number need to treat (NNT), 20; P < 0.05). Use of NSAIDs effectively prevented mild pancreatitis compared with use of placebo (2.5 % vs. 4.1 %; 95 % CI, -0.05 to - 0.01; NNT, 33; P < 0.05), but the information on moderate and severe PEP could not be completely elucidated. Only rectal administration reduced incidence of PEP (6.8 % vs. 13 %; 95 % CI, -0.10 to - 0.04; NNT, 20; P < 0.05). Furthermore, only diclofenac or indomethacin use was effective in preventing PEP. Conclusions Rectal administration of diclofenac and indomethacin significantly reduced risk of developing mild PEP. Further RCTs are needed to compare efficacy between NSAID administration pathways in prevention of PEP after ERCP.
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Affiliation(s)
- Juan Pablo Román Serrano
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Diogo Turiani Hourneaux de Moura
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Wanderley Marques Bernardo
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Igor Braga Ribeiro
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Tomazo Prince Franzini
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Eduardo Turiani Hourneaux de Moura
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | - Vitor Ottoboni Brunaldi
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
| | | | - Paulo Sakai
- Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – HC/FMUSP, Gastrointestinal Endoscopy Unit, São Paulo, Brazil
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Mandalia A, Wamsteker EJ, DiMagno MJ. Recent advances in understanding and managing acute pancreatitis. F1000Res 2018; 7. [PMID: 30026919 DOI: 10.12688/f1000research.14244.1] [Citation(s) in RCA: 25] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 06/20/2018] [Indexed: 12/16/2022] Open
Abstract
This review highlights advances made in recent years in the diagnosis and management of acute pancreatitis (AP). We focus on epidemiological, clinical, and management aspects of AP. Additionally, we discuss the role of using risk stratification tools to guide clinical decision making. The majority of patients suffer from mild AP, and only a subset develop moderately severe AP, defined as a pancreatic local complication, or severe AP, defined as persistent organ failure. In mild AP, management typically involves diagnostic evaluation and supportive care resulting usually in a short hospital length of stay (LOS). In severe AP, a multidisciplinary approach is warranted to minimize morbidity and mortality over the course of a protracted hospital LOS. Based on evidence from guideline recommendations, we discuss five treatment interventions, including intravenous fluid resuscitation, feeding, prophylactic antibiotics, probiotics, and timing of endoscopic retrograde cholangiopancreatography (ERCP) in acute biliary pancreatitis. This review also highlights the importance of preventive interventions to reduce hospital readmission or prevent pancreatitis, including alcohol and smoking cessation, same-admission cholecystectomy for acute biliary pancreatitis, and chemoprevention and fluid administration for post-ERCP pancreatitis. Our review aims to consolidate guideline recommendations and high-quality studies published in recent years to guide the management of AP and highlight areas in need of research.
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Affiliation(s)
- Amar Mandalia
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
| | - Erik-Jan Wamsteker
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
| | - Matthew J DiMagno
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
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Abstract
This review highlights advances made in recent years in the diagnosis and management of acute pancreatitis (AP). We focus on epidemiological, clinical, and management aspects of AP. Additionally, we discuss the role of using risk stratification tools to guide clinical decision making. The majority of patients suffer from mild AP, and only a subset develop moderately severe AP, defined as a pancreatic local complication, or severe AP, defined as persistent organ failure. In mild AP, management typically involves diagnostic evaluation and supportive care resulting usually in a short hospital length of stay (LOS). In severe AP, a multidisciplinary approach is warranted to minimize morbidity and mortality over the course of a protracted hospital LOS. Based on evidence from guideline recommendations, we discuss five treatment interventions, including intravenous fluid resuscitation, feeding, prophylactic antibiotics, probiotics, and timing of endoscopic retrograde cholangiopancreatography (ERCP) in acute biliary pancreatitis. This review also highlights the importance of preventive interventions to reduce hospital readmission or prevent pancreatitis, including alcohol and smoking cessation, same-admission cholecystectomy for acute biliary pancreatitis, and chemoprevention and fluid administration for post-ERCP pancreatitis. Our review aims to consolidate guideline recommendations and high-quality studies published in recent years to guide the management of AP and highlight areas in need of research.
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Affiliation(s)
- Amar Mandalia
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
| | - Erik-Jan Wamsteker
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
| | - Matthew J DiMagno
- Division of Gastroenterology and Hepatology, University of Michigan School of Medicine, Ann Arbor, MI, 48109, USA
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Hamada T, Nakai Y, Lau JY, Moon JH, Hayashi T, Yasuda I, Hu B, Seo DW, Kawakami H, Kuwatani M, Katanuma A, Kitano M, Ryozawa S, Hanada K, Iwashita T, Ito Y, Yagioka H, Togawa O, Maetani I, Isayama H. International study of endoscopic management of distal malignant biliary obstruction combined with duodenal obstruction. Scand J Gastroenterol 2018; 53:46-55. [PMID: 28982258 DOI: 10.1080/00365521.2017.1382567] [Citation(s) in RCA: 22] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/08/2023]
Abstract
OBJECTIVE Endoscopic transpapillary or endoscopic ultrasound (EUS)-guided stent placement is used for nonresectable distal malignant biliary obstruction. We conducted a retrospective study to evaluate endoscopic biliary drainage in patients with duodenal obstruction. METHODS We included consecutive patients who underwent endoscopic biliary drainage combined with a duodenal stent at 16 referral centers in four Asian countries. The primary outcome was time to recurrent biliary obstruction (TRBO). We assessed TRBO according to the sequence of biliary and duodenal obstruction (group 1/2/3, biliary obstruction first/concurrent/duodenal obstruction first, respectively) or the location of duodenal obstruction (type I/II/III, proximal to/affecting/distal to the ampulla, respectively). We also evaluated functional success and adverse events. RESULTS We included 110 patients (group1/2/3, 67/29/14 patients; type I/II/III, 45/46/19 patients; endoscopic retrograde cholangiopancreatography [ERCP]/EUS-guided choledocoduodenostomy/EUS-guided hepaticogastrostomy, 90/10/10 patients, respectively). The median TRBO of all cases was 450 days (interquartile range, 212-666 days) and functional success was achieved in 105 cases (95%). The TRBO did not differ significantly by the timing or location of duodenal obstruction (p = .30 and .79, respectively). The TRBO of metal stents (n = 96) tended to be longer compared with plastic stents (n = 14, p = .083). Compared with ERCP, EUS-guided biliary drainage was associated with a higher rate of adverse events. CONCLUSION Transpapillary or transmural endoscopic biliary drainage with a duodenal stent was effective, irrespective of the timing or location of duodenal obstruction. A prospective study is required considering the tradeoff of technical success rate, stent patency, and adverse events (ClinicalTrials.gov number, NCT02376907).
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Affiliation(s)
- Tsuyoshi Hamada
- a Department of Gastroenterology, Graduate School of Medicine , The University of Tokyo , Tokyo , Japan
| | - Yousuke Nakai
- a Department of Gastroenterology, Graduate School of Medicine , The University of Tokyo , Tokyo , Japan
| | - James Y Lau
- b Department of Surgery , Prince of Wales Hospital, The Chinese University of Hong Kong , Shatin , Hong Kong SAR
| | - Jong Ho Moon
- c Department of Internal Medicine, Digestive Disease Center and Research Institute , Soon Chun Hyang University School of Medicine , Seoul , Korea
| | - Tsuyoshi Hayashi
- d Department of Medical Oncology and Hematology , Sapporo Medical University Hokkaido , Japan.,e Department of Gastroenterology , Hokkaido Cancer Center , Hokkaido , Japan
| | - Ichiro Yasuda
- f First Department of Internal Medicine , Gifu University Hospital , Gifu , Japan.,g Department of Gastroenterology , Teikyo University Mizonokuchi Hospital , Kanagawa , Japan
| | - Bing Hu
- h Department of Endoscopy , Eastern Hepatobiliary Hospital, Second Military Medical University , Shanghai , P.R. China
| | - Dong-Wan Seo
- i Department of Gastroenterology , Asan Medical Center, University of Ulsan College of Medicine , Seoul , Korea
| | - Hiroshi Kawakami
- j Department of Gastroenterology and Hepatology , Hokkaido University Hospital , Hokkaido , Japan.,k Department of Gastroenterology and Hepatology , Center for Digestive Disease University of Miyazaki , Miyazaki , Japan
| | - Masaki Kuwatani
- j Department of Gastroenterology and Hepatology , Hokkaido University Hospital , Hokkaido , Japan
| | - Akio Katanuma
- l Center for Gastroenterology, Teine Keijin-kai Hospital , Hokkaido , Japan
| | - Masayuki Kitano
- m Department of Gastroenterology and Hepatology , Kinki University Faculty of Medicine , Osaka , Japan
| | - Shomei Ryozawa
- n Department of Gastroenterology , Saitama Medical University International Medical Center , Saitama , Japan
| | - Keiji Hanada
- o Department of Gastroenterology , Onomichi General Hospital , Hiroshima , Japan
| | - Takuji Iwashita
- f First Department of Internal Medicine , Gifu University Hospital , Gifu , Japan
| | - Yukiko Ito
- p Department of Gastroenterology , Japanese Red Cross Medical Center , Tokyo , Japan
| | - Hiroshi Yagioka
- q Department of Gastroenterology , Tokyo Metropolitan Police Hospital , Tokyo , Japan
| | - Osamu Togawa
- r Department of Gastroenterology , Kanto Central Hospital , Tokyo , Japan
| | - Iruru Maetani
- s Division of Gastroenterology and Hepatology, Department of Internal Medicine , Toho University Ohashi Medical Center , Tokyo , Japan
| | - Hiroyuki Isayama
- a Department of Gastroenterology, Graduate School of Medicine , The University of Tokyo , Tokyo , Japan
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