Original article

ERCP with the overtube-assisted enteroscopy technique: a systematic review

Authors

Matthew Skinner1, Daniel Popa1, Helmut Neumann1, 2, C. Mel Wilcox1, Klaus Mönkemüller1

Institutions

1

submitted 23. September 2013 accepted after revision 2. March 2014

Background and study aim: Overtube-assisted enteroscopy (OAE) techniques have increased the ability to perform endoscopic retrograde cholangiopancreatography (ERCP) in patients with altered upper gastrointestinal anatomy, such as Roux-en-Y gastric bypass. The aim of this study was to compare the efficacy and safety of OAEERCP in patients with different configurations of upper gastrointestinal anatomy. Patients and methods: A systematic review was performed following a literature search for papers published between 1966 and August 2013. The following databases were searched: MEDLINE (via PubMed), Embase, Cochrane library, and Scopus. The following end points were analyzed: diagnostic and therapeutic success rates, cannulation success rate, ERCP success rate, type of enteroscopy, types of intervention, complications. Results: A total of 23 relevant reports on OAE procedures, including single-balloon, double-balloon, and spiral enteroscopy, were analyzed. Studies included a total of 945 procedures in 679 patients (age 2 – 91 years) who had a variety of postsurgical upper gastrointestinal anatomical configurations. Among patients who underwent Roux-en-Y with gastric bypass, endoscopic success was 80 % and ERCP success was 70 %. In patients who had undergone a Roux-en-Y with

either a pancreaticoduodenectomy, pylorus-preserving pancreaticoduodenectomy, or hepaticojejunostomy, endoscopic success was 85 % and ERCP success was 76 %. In patients who had undergone a Billroth II procedure, endoscopic success was 96 % and ERCP success was 90 %. In patients with native papilla who underwent successful endoscopy, cannulation was successful in 90 % of patients compared with 92 % in patients with an anastomosis. Overall ERCP success for all attempts was approximately 74 %. Interventions included sphincterotomy, pre-cut papillotomy, anastomotic stricturoplasty, stone removal, stent insertion, stent replacement, and balloon dilation of stenotic anastomosis. There were 32 major complications among the 945 procedures (3.4 %). Conclusion: Both endoscopic and ERCP success rates were highest in patients with Billroth II anatomy, followed by those with pancreaticoduodenectomy and Roux-en-Y hepaticojejunostomy; the lowest success rates were in patients with Roux-en-Y gastric bypass. Cannulation rates appeared to be equivalent in patients with both native papilla and biliary-enteric or pancreaticoenteric anastomoses. The diagnostic and therapeutic potential of balloon-assisted ERCP were high and the adverse event rate was low.

Introduction

Shortly after its introduction, evidence emerged demonstrating that DBE was able to facilitate ERCP in patients who had undergone previous upper gastrointestinal surgery that left them with anatomical alterations that rendered the pancreaticobiliary system inaccessible to conventional endoscopy [4]. ERCP success was further demonstrated using the single-balloon enteroscopy (SBE) method [5] and, subsequently, spiral enteroscopy [6]. As all of these methods rely on the use of overtubes, they are collectively called OAE techniques.

Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1365698 Published online: 16.5.2014 Endoscopy 2014; 46: 560–572 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0013-726X Corresponding author Klaus Mönkemüller, MD, PhD Basil I. Hirschowitz Endoscopic Center of Excellence Division of Gastroenterology and Hepatology Endoscopy Unit, JT 664 619 19th Street S Birmingham, AL 35249 USA Fax: +1-205-9341240 [email protected]

Division of Gastroenterology and Hepatology, Basil Hirschowitz Endoscopic Center of Excellence, Birmingham, Alabama, USA 2 Department of Medicine 1, Interdisciplinary Endoscopy, University of Erlangen-Nuremberg, Erlangen, Germany

!

Endoscopic retrograde cholangiopancreatography (ERCP) is an essential tool for therapy of various pancreaticobiliary diseases, with success rates in excess of 95 % in patients with normal anatomy [1]. In contrast, ERCP with conventional equipment in patients with surgically altered anatomy has had limited success, peaking at only 51 % [2]. The introduction of overtube-assisted enteroscopy (OAE) with the double-balloon enteroscopy (DBE) technique revolutionized the endoscopist’s ability to access the small bowel [3].

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

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560

Original article

Methods !

Three investigators (D.P., M.S., and K.M.) independently performed a search of the medical literature from 1966 to August 2013. The following databases were searched: MEDLINE (using the PubMed search engine; www.pubmed.gov), Embase, Cochrane library, and Scopus. To capture all potentially relevant articles with the highest degree of sensitivity, the search terms were intentionally broad. The terms used were: “endoscopic retrograde cholangiopancreatography” or “ERCP” and “double balloon enteroscopy” or “single balloon enteroscopy” or “enteroscopy” or “spiral enteroscopy”; “balloon-assisted ERCP.” Papers were restricted to “full text” in English. A manual search was also conducted on additional sources of information, such as bibliographies of identified articles, abstracts, congress books, and internet searches on the pharmaceutical industry and US Food and Drug Administration web pages. Potentially relevant articles were retrieved and their reference lists were reviewed in order to identify studies that the search strategy may have missed. The authors’ personal archives were also searched to identify additional studies. The abstracts of articles identified in the initial search were independently reviewed by three investigators (D.P., M.S., and K.M.) to determine whether or not they were eligible for inclusion in a full article review. If there was disagreement about whether to include an abstract, the full paper was reviewed. Inclusion criteria for article type were: prospective or retrospective, feasibility, observational or comparative studies, in which OAE was performed with the intention to diagnose and/or treat biliary or pancreatic diseases. Studies were excluded if they included fewer than 10 patients, or were case reports or abstracts.

Definitions Successful enteroscopy (“endoscopic success”) was defined as intubation of the afferent limb and the ability to identify the papilla of Vater or the anastomotic site (biliary-enteric or pancreaticoenteric). Diagnostic success was defined as successful duct cannulation and a successful cholangiogram leading to a diagnosis. ERCP success was defined as a successful enteroscopy with successful diagnostic and therapeutic interventions.

Data analysis Data extraction into evidence tables was carried out by two reviewers (D.P. and M.S.) using standardized forms. Data relating to the following were independently extracted: study design and methods, population, sample size, inclusion and exclusion criteria, patient demographics, patient anatomy, indication for procedure, type of OAE, enteroscopic success, cannulation success, ERCP success, types of intervention, and major complications as identified by the authors of the original work. Discrepancy was resolved by consensus. The reviewed papers presented their results per patient, per procedure, or both. If possible, success rates for endoscopy, cannulation, and ERCP were defined per patient on the data extraction forms; however, if data from the original article were only provided in terms of procedures, they were included in the final analysis and the studies were denoted with an (*). In cases where success rates for endoscopy, cannulation, and ERCP were provided only for a subset of cases, then this is reflected in the tables. After collection, data were summarized into four tables based on patients’ anatomical configuration. Given the wide range and heterogeneity of studies, meta-analytic techniques could not be applied to the data in a valid fashion. For example, across the individual studies, three different types of endoscopic modalities, different inclusion and exclusion criteria, and different methodologies were adopted. Therefore, descriptive statistics were used to summarize the findings. Data presented as pooled estimates do not account for heterogeneity between studies and are reported for explorative purposes only.

Results !

The initial search yielded 253 citations. A total of 23 studies fulfilled the inclusion criteria [5 – 27]. A total of 679 patients (age range 2 – 91 years) with altered postsurgical anatomy underwent 945 OAE-ERCP procedures (1.4 procedures per patient). The procedures were performed for a variety of pancreaticobiliary disorders that required therapeutic intervention, including sphincterotomy, pre-cut papillotomy, anastomotic stricturoplasty, stone removal, stent insertion, stent replacement, and balloon dilation " Tables 1 – 4). (● " Table 1 describes endoscopic and ERCP success in patients who ● " Table 2 deunderwent Roux-en-Y with gastric bypass [6 – 15]. ● scribes endoscopic and ERCP success in patients who underwent Roux-en-Y with pancreaticoduodenectomy, Roux-en-Y with pylorus-preserving pancreaticoduodenectomy, or Roux-en-Y with hepaticojejunostomy, as these procedures are of similar difficulty, and all have anastomotic sites for cannulation [5, 6, 8 – 11, 13, " Table 3 describes endoscopic and ERCP success in 14, 16 – 23]. ● patients who had Billroth II anatomy [8 – 11, 13, 16, 18, 19, 22]. " Table 4 describes cannulation success in those who had native ● papilla and those with an anastomotic site (biliary-enteric or pancreaticoenteric) [5, 6, 9 – 15, 17 – 27]. The variety of surgically altered anatomies included: Billroth II gastric resection, Roux-en-Y with gastric bypass, orthotopic liver transplantation with Roux-en-Y with hepaticojejunostomy, Whipple resection, pylorus-preserving Whipple resection, Roux-en-Y with hepaticojejunostomy,, gastrojejunostomy, chole" Figs. 1 – 6) dochojejunostomy, and pancreaticojejunostomy (● [28 – 31]. Both conscious sedation and propofol sedation or general anesthesia were used successfully during OAE, the prefer-

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

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Despite the increasing use of OAE techniques to perform ERCP in patients with altered upper gastrointestinal anatomy, there are no systematic reviews of these methods. The aim of this study was to undertake a systematic review of OAE techniques for ERCP in patients with surgically altered anatomy to determine the efficacy, feasibility, and safety of the technique. In detail, the aims were: 1) to compare endoscopic and ERCP success rates in patients who had undergone upper gastrointestinal operations, including Billroth II, Roux-en-Y with pancreaticoduodenectomy, Roux-en-Y with pylorus-preserving pancreaticoduodenectomy, Roux-en-Y with hepaticojejunostomy, and Roux-en-Y with gastric bypass; 2) to evaluate the efficacy of cannulation in a native papilla compared with cannulation of the anastomotic site (biliary-enteric or pancreaticoenteric) when utilizing OAE; 3) to compare the endoscopic and ERCP success rates of DBE, SBE, and spiral enteroscopy; and 4) to compare the aggregate efficacy and safety of various OAE techniques.

561

Original article

Table 1 Success of enteroscopy and endoscopic retrograde cholangiopancreatography in patients with Roux-en-Y gastric bypass.

Study, first author

OAE method

[reference]

Table 3 Success of enteroscopy and endoscopic retrograde cholangiopancreatography success in patients with Billroth II anatomy.

Endoscopic

ERCP suc-

Study, first author

OAE

Endoscopic suc-

ERCP success,

success, n/N

cess, n/N

[reference]

method

cess, n/N

n/N

N/A

Cho [8]

sDBE

4/5

Shimatani [9] 1

sDBE

52/55

Cho [8]

sDBE

6/6

50/55

Shimatani [9] 1

sDBE

22/22

N/A 22/22

Siddiqui [10]

sDBE

32/39

29/39

Siddiqui [10]

sDBE

3/3

3/3

Osoegawa [11]

DBE

24/25

21/25

Osoegawa [11]

DBE

18/19

16/19

Choi [12]

DBE

22/28

16/28

Raithel [16]

DBE

0/1

Wang [13]

SBE

6/6

6/6

Aabakken [18]

DBE

1/1

Saleem [14] 1

SBE

10/15

Schreiner [15]

SBE, DBE

23/32

Lennon [6]

Spiral

Shah [7]

DBE, SBE, spiral

Overall (%)

N/A 19/32

Maaser [19]

DBE

2/2

1/2

Wang [13]

SBE

1/1

1/1

SBE

9/18

7/18

Itoi [22]

48/63

39/63

Overall

230/286 (80)

187/266 (70)

OAE, overtube-assisted enteroscopy; (s)DBE, (“short”) double-balloon enteroscopy; SBE, single-balloon enteroscopy; spiral, spiral enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, data not available. 1 Results reported for procedures rather than patients.

2/2

2/2

55/57 (96%)

45/50 (90%)

OAE, overtube-assisted enteroscopy; (s)DBE, (“short”) double-balloon enteroscopy; SBE, single-balloon enteroscopy; spiral, spiral enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, data not available. 1 Results reported for procedures rather than patients.

Table 4 Table 2 Success of enteroscopy and endoscopic retrograde cholangiopancreatography in patients with Roux-en-Y with pancreaticoduodenectomy, pylorus-preserving pancreaticoduodenectomy, or hepaticojejunostomy.

0/1 N/A

Cannulation success in native papilla and hepaticojejunostomy.

Study, first author

OAE

Native papilla,

Anastomosis,

[reference]

method

n/N

n/N

Shimatani [9]

1

sDBE

72/74

26/26

Study, first author

OAE

Endoscopic

ERCP success,

Siddiqui [10]

sDBE

36/40

28/31

[reference]

method

success, n/N

n/N

Osoegawa [11]

DBE

37/42

Cho [8]

sDBE

6/8

0/1

Choi [12]

DBE

18/22

Shimatani [9] 1

sDBE

26/26

26 26

Parlak [17]

DBE

Siddiqui [10]

sDBE

31/32

28/32

Aabakken [18]

DBE

0/1

Osoegawa [11]

DBE

3/3

3/3

Maaser [19]

DBE

3/3

DBE

N/A

3/3 N/A 13/13 11/12 4/5

Raithel [16]

DBE

15/19

14/19

Pohl [20] 1

Parlak [17]

DBE

13/14

12/14

Monkemuller [21]

DBE

1/3

6/7

Aabakken [18]

DBE

11/11

Emmett [24]

DBE

5/6

8/8

Maaser [19]

DBE

Pohl [20] 1

DBE

N/A 21/25

N/A 3/6 21/25

N/A

21/21

Moreels [25]

DBE

3/5

9/9

Chua [26]

DBE

1/1

13/13

Mönkemüller [21]

DBE

6/7

6/7

Neumann [5]

SBE

1/3

6/6

Neumann [5]

SBE

5/8

5/8

Wang [13]

SBE

7/7

6/6

Wang [13]

SBE

4/5

3/5

Saleem [14] 1

SBE

7/10

32/32

Itoi [22]

SBE

8/10

Azeem [23] 1

SBE

Saleem [14]*

SBE

32/41

Itoi [22]

SBE

2/2

2/2

Azeem [23]*

SBE

53/58

44/58

Itoi [27]

SBE

17/36

Lennon [6]

Spiral

Schreiner [15]

SBE, DBE

Lennon [6] Overall (%)

Spiral

23/36 251/295 (85)

N/A

184/242 (76)

OAE, overtube-assisted enteroscopy; (s)DBE, (“short”) double-balloon enteroscopy; SBE, single-balloon enteroscopy; spiral, spiral enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, data not available. 1 Results reported for procedures rather than patients.

Fig. 1

Overall

N/A 15/15 7/9 19/23 240/274 (88%)

2/2 44/53 N/A 17/23 N/A 249/270 (92%)

N/A, data not available; OAE, overtube-assisted enterocopy; (s)DBE, (“short”) doubleballoon enteroscopy; SBE, single-balloon enteroscopy; spiral, spiral enteroscopy. 1 Results reported for procedures rather than patients.

Endoscopic images of hepaticojejunostomy: a, b with small orifice; c with large orifice.

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Original article

563

Fig. 3 Fluoroscopic image of various scope positions inside the afferent limb, following hepaticojejunostomy. a, b Long limb in Roux-en-Y gastric bypass patient with many adhesions. c Cholangiogram in post-liver transplant patient with stenosis of the hepaticojejunostomy. d Balloon dilation of a hepaticojejunostomy stenosis in a liver transplant patient with Roux-en-Y and hepaticojeunostomy.

ence for which appeared to be site dependent (i. e. hospital or endoscopist). In patients with prior Roux-en-Y gastric bypass, endoscopic success was 80 % (230/289) and ERCP success was 70 % (187/266) " Table 1). In patients who underwent pancreaticoduodenect(● omy, Roux-en-Y with pylorus-preserving pancreaticoduodenectomy, or Roux-en-Y with hepaticojejunostomy, enteroscopic success was 85 % (251/295) and ERCP success was 76 % (184/242) " Table 2). In patients with Billroth II anatomy, enteroscopic (●

success was 96 % (55/57) and ERCP success was 90 % (45/50) " Table 3). (● Success rates for cannulation were almost identical between cannulation of native papilla and anastomotic sites: cannulation of native valves was successful in 88 % of patients (240/274), and cannulation of anastomotic sites was successful in 92 % of pa" Table 4). tients (249 270) (● DBE was able to reach the papilla of Vater or anastomosis in 89 % " Tables 5 and 7). Cannulation of attempts (range 73 % – 100 %) (● was successful in 93 % of attempts (range 85 % – 100 %). Overall

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

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Fig. 2 Endoscopic appearance of intact papilla of Vater. a Patient with Billroth II. b Patient with Rouxen-Y gastric bypass. Cannulation can be challenging: entrance of the biliary cannula should be with the papilla at the center (c), or at the 6 o’clock position (d).

Original article

Fig. 4 Commonly reported endoscopic therapies using balloon-assisted endoscopic retrograde cholangiopancreatography. a, b Wire-guided balloon dilation. c Stone extraction. Fig. 5 The stents used for overtube-assisted enteroscopy endoscopic retrograde cholangiopancreatography are of smaller diameter (7 Fr or smaller). Therefore, most endoscopists insert at least two stents (a). b Single-pigtail stents are also available. c, d Using 5-Fr pancreatic stents, a multistenting approach can be employed.

Fig. 6 In cases of large hepaticojejunostomy, a direct cholangioscopy can be performed (a, b). Targeted therapy of specific intrahepatic stenosis can thus be accomplished.

ERCP success for all attempts was approximately 82 % (range 63 % – 95 %). Overall procedure time ranged between 30 and 240 minutes, with 5 – 120 minutes taken to reach the papilla of Vater or anastomosis. When SBE was used, the papilla of Vater or anastomosis was " Tables 6 and reached in 82 % of attempts (range 75 % – 100 %) (● 7). Cannulation was successful in 86 % of cases (range 76 % – 100 %), and overall ERCP success was approximately 68 % (range " Table 6). Overall procedure time ranged from 15 60 % – 100 %) (● to 212 minutes, with 5 – 86 minutes taken to reach the papilla of Vater or anastomosis. Data about the success of spiral enteroscopy is less robust; however, the ability to reach the papilla of Vater was reported to be

" Taas high as 72 %, with overall ERCP success reported as 65 % (● ble 7). Across all studies, there were 32 major complications among 945 procedures (3.4 %). Major adverse events include cholangitis (n = 1), pancreatitis (n = 11), bleeding (n = 3), perforation (n = 13), and death (n = 1), which was attributed to an embolic stroke. Six of the perforations required subsequent surgery.

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564

Biliary stones (48) Biliary strictures (18) Stent removal (5) SOD dysfunction (3) Biliary leak (3) Pancreatic anastomotic stricture (2)

Cholestasis (59 %) Cholangitis (28 %) Choledocholithiasis (13 %) Pancreatic indications (8 %)

Pancreaticobiliary diseases

Raithel [16] 31 patients 86 DBE Median age 64 years (range 47 – 81) Male:female 16:15

Osoegawa [11] 28 patients 47 DBE Median age 74 years (range 54 – 91) Male:female 18:10

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

papilla n/N

transplant

N/A

4/31

26/28

13/31

42/79

53/68

N/A

N/A

N/A

N/A

n/N

Native

Prior liver

96 % (45/47) 1

74 % (23/31) 2

89 % (71/79) 1

97 % (100/103) 1

86 % (25 /29) 1

% (n/N)

success

Endoscopy

91.3 % (21/23) 2

89 % (40/45) 1

93.6 ± 6.8

90 % (64/71) 1

98 % (98/100) 1

Sphincterotomy (14) Stent insertion (24) Stone extraction (14)

Ostium incision (6) Papillotomy (7) Stent insertion (17) Stent exchange (7) Stone extraction (5) Balloon dilation (3)

Sphincterotomy (39) Pancreaticobiliary duct dilation (30) Biliary stent insertion (25) Stone extraction (35) Brushing cytology (3) Stent removal (4)

Stone extraction (47) Nasobiliary drainage (38) Stent insertion (36) Sphincterotomy (31) CDJ dilation (29) Tumor biopsy (10) Nasopancreatic duct drainage (1)

Stone extraction (9) Stent placement(9) Stent removal (8) Dilation of biliary strictures (8) Biliary sphincterotomy (7) Dilation of biliary sphincter (4)

88.8 % (40/40) 1

91.3 % (21/23) 2

100 % (64/64) 1

100 % (98/98) 1

100 % (24 /24) 1

85.1 % (40/47) 1

67.7 % (21/31) 2

81 % (64/79) 2

95 % (98/103) 1

82.8 % (24 /29) 1

% (n/N)

% (n/N) 96 % (24 /25) 1

success,

vention

ERCP

Overall

% (n/N)

Successful Inter-

Intervention (n)

success

Cannulation

111 ± 54

N/A

N/A

70.7 (30 – 117)

minutes

(range),

duration

Mean

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Billroth-II (19) Roux-en-Y (25) Pancreatico-duodenectomy (3)

Billroth-II (8) RYTG (7) Pancreatico-duodenectomy (7) Roux-en-Y with misc. (15)

RYGB (39) Pancreatico-duodenectomy (20) Billroth II (3) Hepaticojejunostomy (3) RYHJ (4) RYGJ (5) RY- CDJ (2) RYPJ (3)

RYTG (36) Billroth II (17) Pancreatico-duodenectomy (15)

Anastomotic stenosis CBD stones

Shimatani [9] 68 patients 103 sDBE Median age: N/A Male:female: N/A

Siddiqui [10] 79 patients 79 sDBE Median age 58 years (range 29 – 86) Male:female 30:39

RYHJ (7) Billroth II (6) RYGJ (5) RYEJ (1) Pancreatico-duodenectomy (1)

Choledocholithiasis (10) Anastomotic stricture (8) Cholangitis (8) Follow-up ERCP (2) Bile leakage (1)

Cho [8] 20 patients 29 sDBE Median age 57.9 years (range 26 – 85) Male: female 10:10

Anatomy (n)

Indication (n)

Studies of double-balloon enteroscopy-assisted endoscopic retrograde cholangiopancreatography.

Study details

Table 5

2.1 % (1/47) 1 Perforation requiring surgery (1)

5.8 % (5/86) 1 Perforation requiring surgery (2) Bleeding (1) Pancreatitis (2)

5% (4/79) 1 Pancreatitis (3) Bleeding, self limiting (1)

5% (5/103) 1 Perforation (5) 1 requiring surgery

0% (0/29) 1

% (n/N)

complications

Major

Original article

565

Choledocholithiasis (1) Cholangitis (6) Liver abscess (2) Biliary pancreatitis (1) Malignant compression (1) Chronic pancreatitis (1) Cholangio-lithiasis (1)

Abnormal LFTs (4) Acute pancreatitis (1) Chronic pancreatitis (2) Cholangitis (2) Pancreaticobiliary pain (5)

Jaundice (14) Pain (1) Bleeding (1)

Maaser [19] 11 patients 16 DBE Median age 62.8 years (range 30 – 78) Male:female 8:3

Emmett [24] 14 patients 20 DBE Median age 47 years (range 27 – 73) Male:female 7:7

Pohl [20] 15 patients 25 DBE Median age 60.2 years (range 25 – 80) Male: female 11:4

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572 1/15

2/14

0/15

6/14

84 % (21/25) 1

85 % (17/20) 1

73 % (8/11) 2

100 % (13/13) 2

92.9 % (13/14) 2

% (n/N)

success

Endoscopy

74.6 ± 25

99 ± 48

N/A

N/A

75 ± 62

minutes

(range),

duration

Mean

100 % (21/21) 1

94 % (16/17) 1

87.5 % (7/8) 2

84.6 % (11/13) 2

100 % (13/13) 2

% (n/N)

success

Cannulation

Stone extraction (5) Pancreaticobiliary duct dilation (11) Stent placement (3) APC (2)

Stone extraction (2) Pancreaticobiliary duct dilation (2) Sphincterotomy (3) Stent placement (2) Stent removal (1)

Sphincterotomy (4) Anastomotic dilation (1) Papillary biopsy (1) Stone extraction (1) Stent insertion (2) Bile aspiration (1)

Stent insertion (2) Stent removal (3) Stone extraction (1)

Stricturoplasty (1) Dilation (1) Stent placement (10) Stent removal (5)

Intervention (n)

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RY-CDJ (15)

RYGB (6) Pancreatico-duodenectomy (4) OLT-HJ (1) OLT-CDJ (1) Pancreatico-jejunostomy (1) Frey procedure (1)

0/11

4/11

1/13

10/13

OLT with Roux-en-Y (10) Roux-en-Y with hemihepat-ectomy (1) Billroth-II (1) RYPG (1)

Anastomotic stricture (3) Biliary stones or sludge (1) Anastomotic necrosis (1) Biliary leak (2) Other (2)

Aabakken [18] 13 patients 18 DBE Median age 53 years (range 2 – 81) Male:female 9:4 RYPG (2) RYTG (1) Billroth-II (2) RYHJ (1) Pancreatico-duodenectomy (1) PPPD (2) RY-CDJ (2)

0/13

2/14

RYHJ (14)

n/N

plant

Jaundice (2) Cholangitis (9) Anastomotic stenosis (1) Stent exchange (7) Broken percutaneous catheter (1) Pruritis (1)

papilla

transn/N

Native

Prior liver

Parlak [17] 14 patients 21 DBE Median age 45.3 years (range 28 – 61) Male:female 6:8

Anatomy (n)

Indication (n)

(Continuation)

Study details

Table 5

100 % (16/16) 1

100 % (6/6) 2

100 % (7/9) 2

100 % (6/6) 2

92.3 % (12/13) 2

% (n/N)

vention

Inter-

Successful % (n/N)

success,

84 % (21/25) 1

80 % (16/20) 1

64 % (7/11) 2

84.6 % (11/13) 2

85.7 % (12/14) 2

0% (0/25) 1

0% (0/20) 1

0% (0/16) 1

0% (0/18) 1

4.76 % (1/21) 1 Retroperitoneal air

complications

ERCP % (n/N)

Major

Overall

566 Original article

Cholestasis (8) Choledocho-lithiasis (1) Cholangitis (2) Stent retrieval (1)

Pancreaticobiliary pathology (15)

Mönkemüller [21] 11 patients 17 DBE Median age 59.7 years (range 36 – 77) Male:female 10:1

Moreels [25] 22 patients 15 DBE Median age 52.8 years (range 21 – 85) Male:female 9:13 Roux-en-Y with biliary anastomosis (10) Roux-en-Y with native papilla (5)

RYTG (2) RYPG (1) RYHJ (1) Hepaticojejunostomy (1) Pancreatico-duodenectomy (3) PPPD (3)

Anatomy (n) n/N

plant

N/A

0/11

5/15

4/11

papilla

transn/N

Native

Prior liver

86.7 % (13/15) 1

94.1 % (16/17) 1

% (n/N)

success

Endoscopy

87.5 % (14/16) 1

92.3 % (12/13) 1

N/A

% (n/N)

success

Cannulation

70 (35 – 240)

minutes

(range),

duration

Mean

Pancreaticobiliary duct dilation (7) Stone extraction (3) Stent insertion (2)

Sphincterotomy (2) Papillectomy (1) Stent insertion (5) Stent retrieval (5) Stone extraction (2) Pancreaticobiliary duct dilation (4)

Intervention (n)

90 % (9/10) 1

81.2 % (13/14) 1

% (n/N)

vention

Inter-

Successful % (n/N)

success,

73.3 % (11/15) 1

76.4 % (13/17) 1

6.6 % (1/15) 1 Perforation (1)

5.8 % (1/17) 1 Perforation requiring surgery (1)

complications

ERCP % (n/N)

Major

Overall

Indication

CBD stones (10) Intrahepatic bile duct stones (1) Gallbladder cancer (1) Anastomotic stricture (1)

Itoi [22] 13 patients 13 SBE 2 DBE Median age 67.5 years (range 36 – 86) Male:female 9:4

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

n/N

n/N

11/13

papilla

transplant

N/A

Native

Prior liver

SBE: 92.3 % (12/13) 1 DBE: 100 % (2/2) 1

% (n/N)

success

Endoscopy

66.4 (25 – 152)

minutes

(range),

duration

Mean

SBE: 83 % (10/12) 1 DBE: 100 % (2/2) 1

% (n/N)

success

Cannulation

Sphincterotomy (8) Stone removal (1) Balloon dilation (9)

Interventions (n)

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Billroth-II (2) RYTG (8) RYPG (1) RYHJ (2)

Anatomy

Studies of single-balloon enteroscopy-assisted endoscopic retrograde cholangiopancreatography.

Study details

Table 6

SBE: 100 % (10/10) 1 DBE: 100 % (2/2) 1

% (n/N)

Intervention

Successful

SBE: 77 % (10/13) 1 DBE: 100 % (2/2) 1

% 9n/N)

success

Overall ERCP

0% (0/13) 1

% (n/N)

plications

Major com-

SBE, single-balloon enteroscopy; (s)DBE, (short) double-balloon enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, not available or not applicable; RY, Roux-en-Y with: HJ, hepaticojejunostomy; GJ, gastrojejunostomy; EJ, esophagojejunostomy; TG, total gastrectomy; GB, gastric bypass; PJ, pancreaticojejunostomy; PG, partial gastrectomy; PPPD, pylorus-preserving pancreaticoduodenectomy; CBD, common bile duct; CDJ, choledochojejunostomy; SOD, sphincter of Oddi; OLT, orthotopic liver transplant; LFT, liver function test. APC, argon plasma coagulation. 1 Data are per procedure. 2 Data are per patient.

Indication (n)

(Continuation)

Study details

Table 5

Original article

567

RYTG (12) RYPG (3)

RY with gastroenterostomy (1) RYPG (5) RYHJ (7) Pancreatico-duodenectomy (2) PPPD (2)

CBD stones (15)

CBD stones (4) Cholangitis (6) Cholestasis (3)

Cholangitis (10) Anastomotic stricture (23) Elevated LFTs (21) Biliary leak (1) Stent removal (2)

Cholangitis (4) Choledocholithiasis (1) Biliary ductal dilation (4) Abnormal LFTs (4) Pancreatitis (2) Biliary stricture (2)

Cholestasis Acute cholangitis Primary sclerosing cholangitis with strictures Choledocholithiasis

Itoi [27] 15 patients 14 SBE 1 DBE Median age 70.9 years (range 58 – 88) Male:female 12:3

Neumann [5] 13 patients 17 SBE Median age 66.5 years (range 25 – 77) Male:female 8:5

Azeem [23] 36 patients 58 SBE Median age 54.4 years (range 18 – 68) Male:female25:11

Wang [13] 13 patients 16 SBE Median age 54 years (range 28 – 82) Male:female 2:11

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

Saleem [14] 50 patients 56 SBE Median age 57 years (range 19–85) Male:female 34:16

n/N

n/N

N/A

4/13

36/36

0/13

15/56

N/A

0/36

4/13

15/15

papilla

transplant

N/A

Native

Prior liver

75% (42/56) 1

81.3 % (13/16) 1

91.4 % (53/58) 1

77 % (10/13) 2

100 % (15/15) 2

% (n/N)

success

Endoscopy

78

100 (30 – 212)

93% (39/42) 1

100 % (13/13) 1

75.9 % (44/58) 1

90 % (9/10) 2

45 (15 – 92)

73 (50 – 102)

N/A

Pancreatico-biliary duct dilation (14) Stone extraction (2) Stent placement Stents removal (5) Sphincterotomy (5)

Pancreatico-biliary duct dilation (4) Stone extraction (2) Sphincterotomy (4) Stent removal (3) Stent placement (2)

N/A

Papillectomy (1) Sphincterotomy (1) Pancreatico-biliary duct dilation (4) Biliary stent insertion (2) Stone extraction (2) Stent retrieval (1)

Sphincterotomy (15) Large balloon dilation (15) Stone extraction (15)

91.3% (21/23) 1

90 % (9/10) 1

100 % (41/41) 1

89 % (8/9) 2

100 % (15/15) 2

% (n/N)

% (n/N)

Successful Intervention

Interventions (n)

success

Cannulation

N/A

minutes

(range),

duration

Mean

66.1% (37/56) 1

75 % (12/16) 2

75.9 % (44/58) 1

62 % (8/13) 2

100 % (15/15) 2

% 9n/N)

success

Overall ERCP

0% (0/56)s

12.5% (2/16) 1 Pancreatitis

0% (0/58) 1

0% (0/13) 2

0% (0/15)p

% (n/N)

plications

Major com-

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SBE, single-balloon enteroscopy; DBE, double-balloon enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, not available or not applicable; RY, Roux-en-Y with: HJ, hepaticojejunostomy; TG, total gastrectomy; GB, gastric bypass; PG, partial gastrectomy; PPPD, pylorus-preserving pancreaticoduodenectomy; CBD, common bile duct; CDJ, choledochojejunostomy; OLT, orthotopic liver transplant; LFT, liver function test. 1 Data are per procedure. 2 Data are per patient.

RYHJ (41) RYGB (15)

Billroth-II (1) RYGB (6) RYPG (1) RYHJ (2) Hepaticojejunostomy (3) Pancreatico-duodenectomy (3)

RY with OLT (36)

Anatomy

Indication

(Continuation)

Study details

Table 6

568 Original article

Cholangitis (9) Choledocholithiasis (3) Biliary stricture (3) Biliary leak (1) Blocked stent (1) Stent removal (1)

Papillary stenosis (19) CBD stone (10) Cancer (2) Pancreatic duct stone (1)

Pancreaticobiliary pathology (34)

Papillary stenosis (20) Biliary stones (16) Anastomotic stenosis (19) Primary sclerosing cholangitis (5) Biliary dilatation (2) Bile leak (1) Chronic pancreatitis (1) Other (9)

Chua [26] 16 patients 23 DBE 2 patients 3 SBE Median age 55 years (range 27 – 83) Male:female 15:6

Schreiner [15] 6 patients 6 SBE 26 patients 26 DBE Median age 53 years Male:female 1:31

Lennon [6] 34 patients 29 SBE 25 Spiral Mean age 52.8 ± 14.4 years Male:female 8:26

Shah [7] 45 SBE patients 27 DBE patients 57 spiral patients Total: 129 patients 180 procedures Median age 54 years (range 20 – 84) Male:female 36:93

RYGB (63) RYHJ (45) Gastrectomy (6) Pancreatico-duodenectomy (10) Other (5)

RYGB (18) Roux-en-Y with other (36)

RYGB

Pancreatico-duodenectomy (1) Billroth-II (1) RY with OLT (12) RYHJ (6) Kasai (1)

Anatomy (n) n/N

n/N

14/129

N/A

0/32

N/A

9/32

32/32

1/18

papilla

transplant

12/18

Native

Prior liver

SBE: 69 % (31/45) 1 DBE: 74 % (20/27) 1 Spiral: 72 % (41/57) 1

59 % 32/54

72 % (23/32) 1

DBE: 75 % (12/16) 1 SBE: 100 % (2/2) 1

% (n/N)

success

Endoscopic

75 % (24/32) 1

SBE: 87 % (27/31) 1 DBE: 85 % (17/20) 1 Spiral: 90 % (37/41) 1

90 – 120 (65/129)

83 % (19/23) 1

106

SBE: 72 ± 34 Spiral: 81.9 ± 34.6

DBE: 100 % (12/12) 1 SBE: 100 % (2/2) 1

N/A

Stent placement (25) Sphincterotomy (23) Papillotomy (21) Papillary balloon dilation (12) Biliary stricture tissue sampling (1) Anastomotic strictureplasty (16) Nonanastomotic stricture dilation (16) Stone extraction (21) Direct cholangioscopy (11)

Stent insertion (3) Stent removal (3) Sphincterotomy (15)

Sphincterotomy Stent insertion Stone extraction

SBE: 87 % (27/27) 1 DBE: 85 % (17/17) 1 Spiral: 90 % (37/37) 1

SBE: 100 % (8/8) 1 Spiral: 87.5 % (7/8) 1

100 % (19/19) 1

DBE: 78 % (7/9) 1 SBE: 100 % (1/1) 1

% (n/N)

SBE: 60 % (27/45) 1 DBE: 63 % (17/27) 1 Spiral: 65 % (37/57) 1

SBE: 48 % 14/29 Spiral: 36 % 9/25

59 % (19/32) 1

DBE: 62.5 % (10/16) 1 SBE: 100 % (2/2) 1

% (n/N)

% (n/N)

success

Interven-

minutes

Overall ERCP

Successful tion

Stent insertion Stent removal Stricture dilation Stone extraction

Interventions (n)

cess

tion suc-

Cannula-

(range),

duration

Mean

5% (16/129) 1 Pancreatitis (5) Bleeding (1) Pain requiring admission (3) Pain requiring physician follow-up (4) Perforation (2) 1 requiring operative management Death from embolic stroke (1)

SBE: 3.5 % (1/29) 1 Perforation Spiral: 0 % (0/25) 1

3.13 % (1/32) Pancreatitis

5.55 % (1/18) Cholangitis

% (n/N)

Major complications

Skinner Matthew et al. ERCP with overtube-assisted enteroscopy … Endoscopy 2014; 46: 560–572

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SBE, single-balloon enteroscopy; DBE, double-balloon enteroscopy; spiral, spiral enteroscopy; ERCP, endoscopic retrograde cholangiopancreatography; N/A, not available or not applicable; RY, Roux-en-Y with: HJ, hepaticojejunostomy; GB, gastric bypass; CBD, common bile duct; OLT, orthotopic liver transplant. 1 Data are per patient 2 Data are per procedure.

Indication (n)

Comparative studies using single-balloon, double-balloon, and spiral enteroscopy for endoscopic retrograde cholangiopancreatography.

Study details

Table 7

Original article

569

Original article

Discussion !

This is the first systematic review to evaluate the feasibility of OAE-ERCP using all available overtube techniques in the setting of altered gastrointestinal anatomy. A total of 679 patients undergoing 945 OAE-ERCP procedures were included in the review, which has enabled important conclusions to be drawn regarding the potential uses and limitations of OAE to perform ERCP. The evaluation of the efficacy and safety of OAE-ERCP in a variety of anatomical settings is important in an era of increased bariatric surgery, especially given the rise of competing modalities, such as laparoscopy-assisted ERCP and ERCP through a gastrostomy tract [32, 33]. From our own experience and that of other experts who perform these procedures, it was felt that the two major components determining ERCP success were the length of the Roux limb (determined predominantly by the underlying operation) and whether the patient had a native papilla or an anastomotic site for cannulation. The underlying anatomy was divided into three subsections: Roux-en-Y with gastric bypass, Billroth II, and a third category that included pancreaticoduodenectomy, Roux-en-Y with pylorus-preserving pancreaticoduodenectomy, and Roux-en-Y with hepaticojejunostomy, which were considered to be comparable. Patients with Roux-en-Y partial gastrectomy and total gastrectomy were also evaluated. Confirming our experience, OAE-ERCP was the least successful in patients with Roux-en-Y gastric bypass and the most successful in patients with Billroth II anatomy. Patients with previous pancreaticoduodenectomy, pylorus-preserving pancreaticoduodenectomy, or Roux-en-Y with hepaticojejunostomy, were in the middle of this continuum. Overall, ERCP success approached 75 % across all modalities and anatomical configurations. Cannulation is believed to be much more difficult in patients with a native papilla [33]; however, results from this systematic evaluation of cannulation attempts in 271 patients with a native papilla and 270 with anastomoses, showed there was less than a 2 % difference between the populations. Thus, despite the perceived difference between the two populations, it was a surprise to find that the cannulation success for intact papilla and hepaticojeunostomy was nearly identical. However, this may not be the final conclusion. It is possible that studies with low success rates were not published. It is also possible that some of the biliarypancreatic anastomoses were not described well in some studies, which would affect results from patients with lateral jejunostomy upstream of hepatico- or pancreaticojejunostomies, which are much more difficult to cannulate during OAE-ERCP [31, 33]. However, in the included series, this surgical alteration was very uncommon. Those who believe that cannulation of the native papilla is more difficult using the OAE-ERCP technique have proposed several explanations as to why this may be so [5, 8]. First, the 200 cm length of the standard DBE enteroscope makes endoscopic manipulation difficult [5, 33]. In addition, many ERCP accessories cannot be used because of the extended length of the scope [5]. Finally, the DBE enteroscope is a forward-facing instrument, which provides suboptimal viewing angles when attempting to perform " Figs. 1 and 2). It should be noted ERCP in a native papilla [33] (● that the short DBE system resolved these first two issues and resulted in cannulation rates of 95 % for both native papilla (108/ 114) and anastomoses (54/57) [8 – 10]. If the results from the short DBE trials are removed from the evaluations, the discrepan-

cy between native papilla and anastomoses widens to 87 % (117/ 135) and 92 % (195/213), respectively. Based on these results, some experts may argue that using short systems is preferable due to increased compatibility with standard ERCP accessories [29, 30, 33]. It should be emphasized that the accessories used for OAE-ERCP with standard length enteroscopes are not widely available in many countries. Moreover, in some countries, such as the USA, only one manufacturer offers a sufficient variety of extra-long devices. In addition, due to the smaller working channel of long or short enteroscopes, the insertion of self-expanding metal stents may be limited. It seems that the advent of a new generation of endoscopes that provide improved viewing angles for ERCP and a wider accessory port, in conjunction with an increased variety of extra-long accessories for OAE-ERCP may improve the rates of both cannulation and ERCP success. Given the imperfect success of OAE-ERCP, it is worth discussing the alternative modalities of ERCP through a gastrostomy tract and laparoscopy-assisted ERCP. Several studies have documented the efficacy of ERCP via gastrostomy or laparoscopy-assisted ERCP in patients with Roux-en-Y gastric bypass [12, 15, 34]. A study comparing the indications and technical outcomes of ERCP via gastrostomy and DBE-ERCP for patients with previous Roux-en-Y gastric bypass found that ERCP via gastrostomy accessed the major papilla in 95 % (42/44) of cases, with cannulation and interventions successful in all 42 cases, whereas in DBEERCP, the success rates of accessing major papilla, cannulation, and therapeutic intervention was 78 %, 63 %, and 56 %, respectively [12]. However, the complications were higher with ERCP via gastrostomy (14.5 %) compared with DBE-ERCP (3.1 %) (P = 0.022) [28]. The authors concluded that ERCP via gastrostomy is more effective than DBE-ERCP in gaining access to the pancreaticobiliary tree in patients with Roux-en-Y gastric bypass, but it is hindered by the gastrostomy maturation delay and a higher morbidity [12]. Another report comparing laparoscopy-assisted ERCP (n = 24) with OAE-ERCP (n = 32) in patients with Roux-en-Y with gastric bypass noted 100 % success rates for endoscopy, cannulation, and ERCP in the laparoscopy-assisted ERCP group but rates of only 72 %, 59 %, and 59 %, respectively, in the OAE-ERCP group [15]. The small sample size was not powered to evaluate complications, but one minor complication was noted in the OAE-ERCP group and two were recorded for the laparoscopy-assisted ERCP group [15]. A cost analysis was included, and the conclusion was that following Roux-en-Y with gastric bypass, patients with a Roux limb plus ligament of Treitz to jejunojejunal anastomosis limb length of less than 150 cm should be offered OAE-ERCP first, and those with longer limbs should proceed directly to laparoscopy-assisted ERCP [15]. It should be noted that the OAE-ERCP success rates of 56 % [12] and 59 % [15] are lower than the 70 % calculated overall from the current data. These findings highlight the need for further studies and consensus meetings with regard to the best approach for this subgroup of patients with anatomically altered upper gastrointestinal anatomy. Although both OAEERCP and percutaneous drainage techniques are acceptable options, no studies comparing these two approaches were found. Studies evaluating both approaches are thus warranted. Finally, the relative safety of OAE-ERCP and low complication rate must be noted. The major complications in these patients were perforation and bleeding. One death was attributed to postoperative embolic stroke. It appears that the risk of complications using OAE-ERCP appears to be considerably lower than that of percuta-

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570

neous transhepatic biliary interventions and of standard ERCP, which are estimated to be about 5 % – 9 % [35]. This is likely to be due to the fact that in a large percentage of these procedures, the ERCP cannot be performed due to endoscopic failure; in addition, in patients with hepaticojejunostomy the incidence of pancreatitis should be negligible, as no pancreatic duct manipulations are performed. Nevertheless, it is known that deep enteroscopy may induce pancreatitis and thus, this complication may be encountered even in the absence of the ampulla of Vater and/or pancreatic duct manipulation. We are not aware of any other study attempting to summarize the complication rates of OAE-ERCP, and thus, we believe that the current data provide a useful parameter to categorize risk. Furthermore, no studies have prospectively attempted to collect data on OAE-ERCP-associated complications. Thus, future multicenter studies that investigate complications are needed. A potential limitation of the current study should be discussed. The studies included in the analysis were heterogenic, mainly because there are several options for OAE-ERCP, including SBE, DBE, and spiral enteroscopy methods; however, the equivalency of overtube-assisted methods has been well demonstrated [7]. In summary, this systematic review shows that the introduction of OAE has provided improved control to endoscopy operators, and thus, when combined with ERCP, may provide new opportunities for success in both the diagnosis and treatment of pancreaticobiliary disease in patients with altered gastrointestinal anatomy. The success rates appear to be independent of the method used (DBE, SBE or spiral enteroscopy). However, short systems appear to improve therapeutic success, possibly due to the larger working channel of the scope. Currently, the variations in surgically altered anatomy significantly contribute to the success rate of the procedure, with success in patients with Roux-en-Y gastric bypass being limited to 70 % and Billroth II success being as high as 90 %. However, after extensive evaluation, the presence of a biliary-enteric or pancreaticoenteric anastomosis vs. a native papilla does not seem to influence diagnostic and therapeutic success. We believe that the interventional value of the OAE-ERCP could be further improved by expanding the currently limited availability of accessories, and by developing a long ERCP endoscope that is compatible with the overtube system. Further studies comparing the short endoscope systems with the traditional enteroscopes are warranted. In addition, prospective or larger multicenter studies comparing the therapeutic success rate of OAE-ERCP with that of laparoscopy-assisted ERCP in patients with Roux-en-Y gastric bypass are needed. Competing interests: None

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Original article

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Correction Holleran Grainne, Leen Ronan, O'Morain Colm et al. Colon capsule endoscopy as possible filter test for colonoscopy selection in a screening population with positive fecal immunology. Endoscopy 2014: 46: 473–478. Figures 1 and 2 fall under the legend for figure 1 (polyps visualized on colon capsule), figure 3 should have the legend from figure 2 (false positive polyp on colon capsule endoscopy) and the legend from figure 3 as it stands refers to a flow diagram that was not included in the published version.

Population (n = 10,000)

FIT Uptake = 50 % (n = 5,000)

Positivity = 10 % (n = 500)

> 90 % CCE Uptake (n = 450)

CCE Negative (n = 135) False Negative (n = 13) CCE Positive (n = 315)

OC Negative (n = 63) OC Positive (n = 252)

Fig. 3 Expected outcome based on colon capsule endoscopy (CCE) as a filter test in a fecal immunological test (FIT)-based screening program.

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