Algorithm for the multidisciplinary management of hemorrhage in EUS-guided drainage for pancreatic fluid collections

Table 1 Detailed outcome measures for endoscopic ultrasound-guided drainage of pancreatic fluid collections

Study	Year	Country	Design	Single/multi-center	Stent style	No.	PFC style	Technical success	Clinical success	Adverse events	Mortality	Cause of death	Follow-up period
Lang et al[38]	2018	United States	RS	Single	LAMS	19	PPC/WON	99%	94%	53%	5%	Due to bleeding from splenic artery pseudoaneurysms	≥ 6 mo
					DPPS	84	PPC/WON	99%	96%	11%	0%
Aburajab et al[10]	2018	United States	RS	Single	LAMS with no DPPS	46	PPC	96%	91%	25%	0%	None	2-4 mo
					LAMS with DPPS	23	PPC	100%	100%	0%	0%
Siddiqui et al[46]	2017	United States	RS	Multi	LAMS	86	WON	97.70%	90%	12%	0%	None	≥ 6 mo
					DPPS	106	WON	99%	81%	15%	0%
					FCSEMS	121	WON	100%	95%	2%	0%
Bapaye et al[13]	2017	India	RS	Single	BFMS	72	WON	100%	94%	6%	4%	Died from sepsis; organ failure; pulmonary embolism	2 mo
					MPS	61	WON	100%	74%	36%	7%
Bang et al[50]	2017	United States	RCT	Single	LAMS	12	WON	NR	NR	50%	0%	None	4-6 wk
					DPPS	9	WON	NR	NR	0%	0%
Bang et al[6]	2017	United States	RS	Single	LAMS	20	PPC/WON	100%	95%	10%	5%	Died of progressive sepsis	1-2 yr
					DPPS	40	PPC/WON	100%	93%	13%	0%
Lakhtakia et al[54]	2016	India	RS	Single	FCSEMS	205	WON	99.00%	75%	4%	0%	None	12 mo
Sharaiha et al[7]	2016	United States	RS	Multi	LAMS	124	WON	100%	86%	19%	0%	None	3 mo
Gornals et al[11]	2016	Spain	RS	Single	LAMS	12	WON	100%	100%	33%	0%	None	13 ± 11.4 mo
Siddiqui et al[31]	2016	United States	RS	Multi	LAMS	82	PPC/WON	86% PPC 100% WON	100% PPC 88% WON	10%	0%	None	6 mo
Ang et al[20]	2016	Singapore	RS	Multi	FCSEMS	12	PPC/WON	100%	92%	NR	NR	NR	NR
					DPPS	37	PPC/WON	100%	65%	5%	NR
Vazquez-Sequeiros et al[39]	2016	Spanish	RS	Multi	FCSEMS	211	PPC/WON	97%	94%	21%	NR	NR	≥ 6 mo
Shah et al[41]	2015	United States	PS	Single	LAMS	33	PPC/WON	91%	93%	12%	NR	NR	11 mo
Walter et al[45]	2015	The Netherlands	PS	Single	LAMS	61	PPC/WON	98%	93%PPC 81%WON	9%	1%	Died from an unrelated cause (myocardial infarction	4 mo
Sharaiha et al[47]	2015	United States	RS	Multi	FCSEMS	112	PPC	98%	98%	16%	0%	None	≥ 1 yr
					DPPS	118	PPC	92%	89%	31%	0%
Rinninella et al[44]	2015	Italy	RS	Multi	FCSEMS	69	PPC/WON	99%	93%	5%	4%	Died because of multi-organ failure and massive bleeding	10 mo
Mukai et al[14]	2015	Japan	RS	Single	FC BFMS	43	WON	100%	98%	7%	7%	Because of bleeding	1-2 yr
					DPPS	27	WON	100%	93%	19%	0%
Lee et al[55]	2014	South Korea	PS	Single	FCSEMS	25	PFC	100%	87%	0%	0%	None	6-7 mo
					DPPS	25	PFC	100%	91%	8%	0%
Yamamoto et al[56]	2013	Japan	RS	Single	FCSEMS	9	PPC/WON	100%	78%	22%	10%	Because of multiple organ failure	2 mo
Bang et al[63]	2013	United States	RS	Multi	MTGT	76	WON	NR	70%	15%	15%	Due to portal hypertension	1-2 yr
Puri et al[48]	2012	India	PS	Single	DPPS	40	PPC	100%	98%	8%	0%	None	48 mo
Itoi et al[12]	2012	Japan	RS	Single	LAMS	15	PPC	100%	100%	0%	0%	None	11 mo
Varadarajulu et al[27]	2011	United States	RS	Single	DPPS	211	PPC/WON	NR	85%	8%	1%	Due to delayed bleeding	1-2 yr
Varadarajulu et al[64]	2011	United States	RS	Single	MTGT	12	WON	100%	92%	0%	0%	None	5 mo

PPC: Pancreatic pseudocyst; WON: Walled-off necrosis; PFC: Pancreatic fluid collections; PS: Prospective study; RS: Retrospective study; RCT: Randomized controlled trial; Single: Single-center; Multi: Multi-center; FCSEMS: Fully covered self-expandable metal stent; LAMS: Lumen-apposing metal stents; DDPS: Double-pigtail plastic stents; BFMS: Fully covered bi-flanged metal stents; MPS: Multiple plastic stents; MTGT: Multiple transluminal gateway technique; NR: Not reported.

Table 2 Details of the adverse events associated with endoscopic ultrasound-guided drainage of pancreatic fluid collections

Study	Year	Country	Design	Single/multi-center	Stent style	No.	PFC style	Infection	Bleeding	Perforation	Migration	Occlusion	Other adverse events
Lang et al[38]	2018	United States	RS	Single	LAMS/DPPS	103	80 PP 23 WON	0%	5%	1%	0%	0%	13% Unplanned endoscopy
Aburajab et al[10]	2018	United States	RS	Single	LAMS with DPPS/with no DPPS	46	PP	9%	0%	2%	15%	0%	9% Re-intervention
Siddiqui et al[46]	2017	United States	RS	Multi	LAMS/ DPPS/ FCSEMS	313	WON	3%	3%	2%	1%	8%	12% (No details)
Bapaye et al[13]	2017	India	RS	Single	BFMS / MPS	133	WON	2%	5%	0%	2%	0%	14% Persistent sepsis
Bang et al[50]	2017	United States	RCT	Single	LAMS/ DPPS	21	WON	0%	14%	0%	0%	0%	2% Buried stent 5% Biliary stricture
Bang et al[6]	2017	United States	RS	Single	LAMS/ DPPS	60	21 PP 39 WON	12%	0%	0%	5%	0%	28% Re-intervention
Lakhtakia et al[54]	2016	India	RS	Single	FCSEMS	205	WON	0%	3%	1%	1%	10%	1% Buried stent
Sharaiha et al[7]	2016	United States	RS	Multi	LAMS	124	WON	6%	3%	0%	6%	6%	19% Re-intervention
Gornals et al[11]	2016	Spain	RS	Single	LAMS	12	WON	17%	17%	0%	0%	0%	None
Siddiqui et al[31]	2016	United States	RS	Multi	LAMS	82	14 PPC 68 WON	6%	7%	0%	0%	5%	2% Stent maldeployment; 1% pneumoperitoneum
Ang et al[20]	2016	Singapore	RS	Multi	FCSEMS / DPPS	49	WON 14 PP 35	2%	4%	2%	0%	0%	2% Pneumoperitoneum
Vazquez-Sequeiroset et al[39]	2016	Spain	RS	Multi	FCSEMS	211	112 PP 99 WON	23%	7%	-	5%	0%	3% Perforation/pneumoperitoneum
Shah et al[41]	2015	United States	PS	Multi	LAMS	33	PPC/WON	6%	0%	0%	3%	0%	None
Walter et al[45]	2015	The Netherlands	PS	Multi	LAMS	61	PPC/WON	7%	0%	2%	0%	0%	None
Sharaiha et al[47]	2015	United States	RS	Multi	FCSEMS	112	PPC	14%	4%	3%	1%	7%	None
Rinninella et al[44]	2015	Italy	RS	Multi	FCSEMS	93	WON 52 PPC18 PA 19 APFC 4	1%	1%	1%	1%	0%	1% Pneumoperitoneum
Mukai et al[14]	2015	Japan	RS	Single	FC BFMS / DPPS	70	WON	0%	4%	1%	4%	0%	1% Mediastinal emphysema
Lee et al[55]	2014	South Korea	PS	Single	FCSEMS/ DPPS	50	PFC	0%	2%	0%	4%	0%	None
Yamamoto et al[56]	2013	Japan	RS	Multi	FCSEMS	9	5 PPC 4 WON	0%	11%	0%	11%	0%	None
Bang et al[63]	2013	United States	RS	Multi	MTGT	76	WON	8%	1%	1%	4%	0%	None
Puri et al[48]	2012	India	PS	Single	DPPS	40	40 PPC	3%	3%	0%	0%	0%	3% Pneumoperitonium
Itoi et al[12]	2012	Japan	RS	Single	LAMS	15	9 PPC 6 WON	0%	20%	0%	7%	0%	None
Varadarajulu et al[27] (Endo Trans Dra of pfc)	2011	United States	RS	Single	DPPS	211	154 PPC 57 WON	3%	1%	1%	1%	0%	None

PPC: Pancreatic pseudocyst; WON: Walled-off necrosis; PFC: Pancreatic fluid collections; PS: Prospective study; RS: Retrospective study; RCT: Randomized controlled trial; Single: Single-center; Multi: Multi-center; FCSEMS: Fully covered self-expandable metal stent; LAMS: Lumen-apposing metal stents; DDPS: Double-pigtail plastic stents; BFMS: Fully covered bi-flanged metal stents; MPS: Multiple plastic stents; MTGT: Multiple transluminal gateway technique; NR: Not reported.

Table 3 Details of hemorrhage associated with endoscopic ultrasound-guided drainage of pancreatic fluid collections

Study	Year	Country	Design	Center	Stent style	No.	PFC style	Location of drainage	Age	Male	Bleeding rate	Cause and treatment of bleeding	Diagnosis of bleeding
Lang et al[38]	2018	United States	RS	Single	LAMS	19	PPC/WON	TG	51.6	NR	19%	1 Splenic artery pseudoaneurysms-left gastric and splenic artery embolization after cyst-gastrostomy; 2 Collateral vessel bleed-conservative transfused blood; 3 Intracavitary variceal bleed-endoscopically using balloon tamponade	NR
					DDPS	84	PP C/WON	TG/TD	51.6	NR	1%	Stent erosion into the gastric wall-EGD was performed, and a visible vessel was treated with cautery for durable hemostasis	NR
Siddiqui et al[46]	2017	United States	RS	Multi	LAMS	86	WON	TG/TD/Multiport	51.5	89%	7%	Related to stent erosion into a vessel as the WON cavity wall collapses or related to pseudoaneurysm in the cavity wall-significant hemorrhage treated by coil embolization by interventional radiology	NR
					DDPS	106	WON	TG/TD/Multiport	56.3	64%	2%	Due to inadvertent puncture of an artery; another was not reported-Successfully treated with coil embolization by interventional radiology	NR
					FCSEMS	121	WON	TG/TD/Multiport	51.9	79%	0%	None	None
Bapaye et al[13]	2017	India	RS	Single	BFMS	72	WON	Mostly TG	43.8	86%	3%	Because of erosion of the splenic artery by the indwelling inner end of the stent-treated by blood transfusion; splenic artery arteriography embolization	Angiograms
					MPS	61	WON	Mostly TG	40.6	88%	8%	Because of tract dilatation-Blood transfusion; endoscopic clip application; surgery	Angiograms
Bang et al[50]	2017	United States	RCT	Single	LAMS	12	WON	NR	NR	NR	25%	With the resultant friction against regional vasculature surrounding the necrotic cavity precipitating bleeding-Blood transfusions interventional radiology-guided coil embolization	EUS and CT angiograms
					DDPS	9	WON	NR	NR	NR	0%	None	None
Lakhtakia et al[54]	2016	India	RS	Single	FCSEMS	205	WON	NR	34.8	88%	3%	No details of the cause of bleeding-Minor bleeding was self-limiting; major bleeding treated by selective coil embolization; another major bleeding treated by surgery	Abdominal angiography
Siddiqui et al[31]	2016	United States	RS	Multi	LAMS	82	PPC/WON	TG/TD	53.1	67%	7%	No details of the cause of bleeding-Self-limited bleeding	NR
Ang et al[20]	2016	Singapore	RS	Multi	FCSEMS	12	PPC/WON	NR	50	58%	0%	None	None
					DPPS	37	PPC/WON	NR	56	49%	5%	No details of the cause of bleeding-Treated by blood transfusion	NR
Vazquez-Sequeiros et al[39]	2016	Spanish	RS	Multi	FCSEMS	211	PPC/WON	TG/TD	58.1	69%	7%	Portal hypertension due to splenic vein thrombosis and antithrombotic drug therapy in the presence of stent-induced ulceration may have been responsible-Interventional radiology embolization; surgical intervention; repeated endoscopic treatments (sclerotherapy); percutaneous radiology-guided drainage	NR
Sharaiha et al[7]	2016	United States	RS	Multi	LAMS	124	WON	NR	54.2	61%	2%	No details of the cause of bleeding-Embolization by interventional radiology	NR
Sharaiha et al[47]	2015	United States	RS	Multi	ECSEMS	112	PPC	TG/TD	53.2	55%	4%	Significant bleeding due to inadvertent puncture of an artery-Successfully treated with coil embolization by interventional radiology	NR
					DDPS	118	PPC	TG/TD	52.2	69%	NR	NR	NR
Gornals et al[11]	2015	Spain	RS	Single	LAMS	12	WON	TG/TD	52.6	75%	17%	All fluid is evacuated and the cavity lumen is collapsed, or due to a vessel injury from the inner stent end-Arteriography plus endoscopic treatment	Abdominal angiography
Rinninella et al[44]	2015	Italy	RS	Multi	FCSEMS	93	PFC	TG/TD	60	76%	1%	Massive bleeding related to the concomitant use of a NCDC-Surgery	NR
Mukai et al[14]	2015	Japan	RS	Single	FC BFMS	43	WON	NR	54.4	86%	5%	The specific reason for bleeding is unclear-No details regarding the treatment of the bleeding events	NR
					Plastic	27	WON	NR	55.9	78%	0%	None	None
Lee et al[55]	2014	South Korea	PS	Single	FCSEMS	25	PFC	TG/TD	53.7	88%	0%	None	None
					DDPS	25	PFC	TG/TD	51.6	76%	4%	NR	NR
Yamamoto et al[56]	2013	Japan	RS	Single	FCSEMS	9	PPC/WON	TG	45	67%	11%	The bleeding was caused by vessel damage because of inflammation-Trans-arterial embolization	Angiography
Bang et al[63]	2013	United States	RS	Multi	MTGT	53	WON	TG/TD	53	69%	2%	No details of the cause of bleeding-Coil embolization under radiological guidance	NR
Puri et al[48]	2012	India	PS	Single	DPPS	40	PPC	TG/TD	39	78%	3%	Pseudoaneurysm of the blood vessel in the cystic wall ruptured-Surgery	NR
Itoi et al[12]	2012	Japan	RS	Single	LAMS	15	PPC	TG/TD	55.4	80%	20%	No details of the cause of bleeding-Minor, self-limited	None
Varadarajulu et al[27]	2011	United States	RS	Single	DDPS	211	PPC/WON	TG/TD/TE/TJ	52	61%	1%	No details of the cause of bleeding-Required embolization with interventional radiology; conservatively	NR
Varadarajulu et al[64]	2011	United States	PS	Single	DDPS	110	PPC/WON	TG/TD	NR	NR	1%	Coagulant disorder (with underlying acquired factor VIII inhibitors) -Conservative treatment	Arteriography
Talreja et al[53]	2008	United States	PS	Single	FCSEMS	18	PFC	TG/TD	51	67%	13%	Bleeding from the pseudocyst wall-Treated with balloon tamponade and arterial embolization	NR

PPC: Pancreatic pseudocyst; WON: Walled-off necrosis; PFC: Pancreatic fluid collections; PS: Prospective study; RS: Retrospective study; RCT: Randomized controlled trial; Single: Single-center; Multi: Multi-center; FCSEMS: Fully covered self-expandable metal stent; LAMS: Lumen-apposing metal stents; DDPS: Double-pigtail plastic stents; BFMS: Fully covered bi-flanged metal stents; MPS: Multiple plastic stents; MTGT: Multiple transluminal gateway technique; TG: Trans-gastric route; TD: Trans-duodenal route; TE: Trans-esophageal route; TJ: Trans-jejunal route; CT: Computed tomography; EUS: Endoscopic ultrasound; NCDC: Nasocystic drainage catheter; NR: Not reported.

Table 4 Details of clinical outcomes between cautery and non-cautery dilator in endoscopic ultrasound-guided drainage for pancreatic fluid collections

Study	Year	Country	Design	Center	Stent style	No.	PFC style	Overall Technical success	Overall Clinical success	Overall bleeding rate	Dilated approaches (A. balloon/tapered dilator; B. needle knife; C. cystotome catheter; D. ERCP cannula)	Cautery dilator
Lang et al[38]	2018	United States	RS	Single	LAMS/DDPS	103	PPC/WON	99%	95%	5%	A + B	YES
Siddiqui et al[46]	2017	United States	RS	Multi	LAMS/ DDPS/ FCSEMS	313	WON	99%	90%	3%	A + B	YES
Bapaye et al[13]	2017	India	RS	Single	BFMS/MPS	133	WON	100%	82%	5%	A + C	YES
Lakhtakia et al[54]	2016	India	RS	Single	FCSEMS	205	WON	99%	75%	3%	A + C	YES
Siddiqui et al[31]	2016	United States	RS	Multi	LAMS	82	PPC/WON	86% PPC 100% WON	100% PPC 88% WON	7%	A + B	YES
Ang et al[20]	2016	Singapore	RS	Multi	FCSEMS/ DPPS	49	PPC/WON	100%	96%	4%	A + B + C	YES
Vazquez-Sequeiros et al[39]	2016	Spanish	RS	Multi	FCSEMS	211	PPC/WON	97%	94%	7%	A + B + C	YES
Sharaiha et al[7]	2016	United States	RS	Multi	LAMS	124	WON	100%	86%	3%	A + B + C	YES
Sharaiha et al[47]	2015	United States	RS	Multi	ECSEMS/ DDPS	230	PPC	96%	90%	4%	A + B	YES
Gornals et al[11]	2015	Spain	RS	Single	LAMS	12	WON	100%	100%	17%	A + C	YES
Mukai et al[14]	2015	Japan	RS	Single	FC BFMS/Plastic	70	WON	100%	96%	4%	A + C	YES
Lee et al[55]	2014	South Korea	PS	Single	FCSEMS/ DDPS	50	PFC	100%	10%	2%	A + B	YES
Puri et al[48]	2012	India	PS	Single	DPPS	40	PPC	100%	98%	3%	A + B	YES
Itoi et al[12]	2012	Japan	RS	Single	LAMS	15	PPC	100%	100%	20%	A + C	YES
Bang et al[50]	2017	United States	RCT	Single	LAMS/DDPS	21	WON	NR	NR	14%	A	NO
Rinninella et al[44]	2015	Italy	RS	Multi	FCSEMS	93	PFC	99%	93%	1%	A	NO
Yamamoto et al[56]	2013	Japan	RS	Single	FCSEMS	9	PPC/WON	100%	78%	11%	A	NO
Bang et al[63]	2013	United States	RS	Multi	MTGT	53	WON	NR	70%	1%	A	NO
Varadarajulu et al[27]	2011	United States	RS	Single	DDPS	211	PPC/WON	NR	85%	1%	A + D	NO
Varadarajulu et al[65]	2011	United States	PS	Single	DDPS	110	PPC/WON	100%	92%	1%	A + D	NO
Talreja et al[53]	2008	United States	PS	Single	FCSEMS	18	PFC	95%	78%	13%	A	NO

PPC: Pancreatic pseudocyst; WON: Walled-off necrosis; PFC: Pancreatic fluid collections; PS: Prospective study; RS: Retrospective study; RCT: Randomized controlled trial; Single: Single-center; Multi: Multi-center; FCSEMS: Fully covered self-expandable metal stent; LAMS: Lumen-apposing metal stents; DDPS: Double-pigtail plastic stents; BFMS: Fully covered bi-flanged metal stents; MPS: Multiple plastic stents; MTGT: Multiple transluminal gateway technique; ERCP: Endoscopic retrograde cholangiopancreatography; NR: Not reported.