Near-infrared fluorescence guided esophageal reconstructive surgery: A systematic review

Table 1 Demographic data and study characteristics

Ref.	Enrollment	Study design	Non ICG group	No. of patients (M/F)	Median age (range)	Neoadjuvant therapy	Operative technique	Dye and dose	Timing of ICGA	Imaging system	Change of procedure	MINOR score
Shimada et al[40]	2008-2011 (Japan)	Prospective cohort	No	36 GT (29/7)	67 (49-81)	8 CT	Open surgery	2.5 mg Diagnogreen	After GT creation	PDE	Superdrainage (5)	6a
		Feasibility				1 RT	Cervical AS
						1 CRT
Kubota et al[18]	2010-2011 (Japan)	Prospective cohort	No	4 GT (3/1)	69 (64-71)	4 CT	Open surgery	0.5 g/kg	After GT creation	HEMS	No	4a
		Feasibility					Cervical AS
Murawa et al[19]	2009-2010 (Poland)	Prospective cohort	No	15 (13/2)	Mean 56 (54-74)	0	Not reported	25 mg	After GT creation	ICView	End-to-end (4)	6a
		Feasibility					Cervical AS
							Transhiatal
Pacheco et al[20]	2010-2011 (United States)	Retrospective cohort	No	11 (NR)	Mean 56 (SD ± 9)	7 CRT	Open surgery	Not reported	After GT creation	SPY	No	4a
		Feasibility		- 10 ICGA good AS			Cervical AS
				- 1 ICGA poor AS			Transhiatal
Kumagai et al[21]	2013 (Japan)	Prospective cohort	No	20 (16/4)	Mean 68 (50-79)	0	Open surgery	2.5 mg Diagnogreen	After GT creation	PDE	No	13a
		Feasibility					Cervical AS
Rino et al[22]	2009-2013 (Japan)	Prospective cohort	No	33 (29/4)	Mean 68 (NR)	Not reported	Not reported	2.5 mg Diagnogreen	After GT creation	PDE	No	4a
		Feasibility					Thoracic AS
							Ivor Lewis
Sarkaria et al[23]	2012-2013 (United States)	Prospective cohort	No	30 (22/8)	59 (37-76)	24 CRT	RAMIE	10 mg	Before GT creation	FireFly	No	6a
		Feasibility					Cervical + thoracic AS
							Ivor Lewis + McKeown
Hodari et al[25]	2011-2014 (United States)	Retrospective cohort	Yes	54 (44/10)	65 (45-81)	38 CRT	RAMIE	Not reported	Before anastomosis during anastomosis	FireFly	Guided AS (39)	6b
		Historical case control		- 39 ICGA			Thoracic AS
				- 15 non ICGA			Ivor Lewis
Campbell et al[26]	2007-2013 (United States)	Retrospective cohort	Yes	90 (74/16)	62 (22-81)	6 CT	MIE + Hybrid + Open	5 mg	After GT creation	SPY	Guided AS (21)	15b
		Historical case control		- 21 ICGA		54 CRT	Thoracic AS
				- 60 non ICGA			Ivor Lewis
				- 9 Doppler
Yukaya et al[27]	2013-2014 (Japan)	Prospective cohort	No	27 (26/1)	67 (40-86)	Not reported	Not reported	0,1 mg/kg Diagnogreen	After GT creation	HEMS	No	11a
		Feasibility					Cervical AS
Zehetner et al[28]	2008-2011 (United States)	Prospective cohort	No	150 (125/25)	67 (IQR 57-74)	67 CRT	MIE + Open Cervical AS	2.5 mg	After GT creation	SPY	Guided AS (95)	13b
		Case controlled		- 6 delayed AS = excluded			Transhiatal + McKeown
				- 95 ICGA good AS
				- 49 ICGA poor AS
Koyonagi et al[30]	2014-2015 (Japan)	Prospective cohort	No	40 (34/6)	68 (26-82)	11 CT	Not reported	2.5 or 1.25 mg Diagnogreen	After GT creation	PDE	No	17b
		Case controlled		- 25 ICGA good AS		4 CRT	Cervical AS
				- 15 ICGA poor AS
Schlottmann et al[33]	NR (United States)	Prospective cohort	No	5 (3/2)	59 (56-70)	1 CRT	Hybrid	5 mg	Before anastomosis	IMAGE1	Guided AS (5)	8a
		Feasibility					Thoracic AS	ICG-pulsion			- Resection (2)
							Ivor Lewis
Kitagawa et al[29,34]	2011-2017 (Japan)	Retrospective cohort	No	72 (57/15)	Mean 66 (SD ±7)	60 CT	MIE + Hybrid	5 mg	Before GT creation	HEMS	Guided AS (26)	18b
		Case controlled		- 26 ICGA		2 CRT	Cervical AS		After GT creation		Guided GT (46)
				- 46 ICGA-LMM			McKeown				- End-to-end (4)
				(line marking method)							- Superdrainage (1)
Ohi et al[32,35]	2000-2015 (Japan)	Retrospective cohort	Yes	120 (101/19)	68 (IQR 63-74)	56 Not reported	Open + Hybrid	2.5 mg Diagnogreen	After GT creation	PDE	Guided AS 60 s (59)	15b
		Historical case control		- 59 ICGA			Cervical AS				- End-to-end (3)
				- 61 non ICGA							- Supercharge/drain (1)
											- Manubriotomy (5)
Karampiris et al[36]	2010-2016 (Germany)	Retrospective cohort	Yes	90 (65/23 + 2 NR)	Mean 62 (SD ± 9)	69 CT	Open + Hybrid	7.5 mg	After GT creation	PinPoint	Guided AS (33)	16b
		Historical case control		- 35 ICGA		25 RT	cervical + thoracic AS				- Resection (26)
				- 33 ICGA good AS			Thoracophrenico + McKeown
				- 2 ICGA poor AS
				- 55 non ICGA
Noma et al[37]	2010-2016 (Japan)	Retrospective cohort	Yes	285 (244/41)	Mean 65 (SD ± 8)	129 CT	Open+ Hybrid + MIE	12.5 mg Diagnogreen	After GT creation	PDE	Guided AS 30 s (71)	17b
		Historical case control		- 71 ICGA		21 CRT	Cervical AS				- extended mobilization
		Case matched		- 214 non ICGA			McKeown				-Supercharge/drain (1)
Dalton et al[38]	2014-2016 (United States)	Retrospective cohort	Yes	40 (32/8)	Mean 64 (SD ± 10)	36 Not reported	MIE	7.5 mg	After GT creation	PinPoint	Guided AS (20)	17b
		Historical case control		- 20 ICGA			Thoracic AS				- Resection (6)
				- 20 non ICGA			Ivor Lewis
Kumagai et al[39]	2014-2017 (Japan)	Prospective cohort	No	70 (59/11)	71 (46-82)	Not reported	Not reported	2.5 mg Diagnogreen	After GT creation	PDE	Guided AS 90 s (70)	8a
		Feasibility					Cervical AS				- Resection (35)

Neoadjuvant treatment: CT: Chemotherapy, RT: Radiotherapy, CRT: Chemo radiation; Fluorescent imaging system: PDE: Photodynamic Eye; Hamamatsu Photonics K.K, Hamamatsu, Japan; HEMS: Hyper Eye Medical System; Mizuho Ikakogyo Co., Tokyo, Japan; ICView: Pulsion Medical Systems, Munich, Germany; SPY: SPY Imaging System, Novadaq Industries Inc., Toronto, Canada; FireFly: Firefly Fluorescence Imaging Scope, Intuitive Surgical, Sunnyvale, Canada; IMAGE1: IMAGE1 STORZ professional image enhancement system; PinPoint: PinPoint system, Novadaq, Ontario, Canada; ICGA: Indocyanine green fluorescence angiography; AL: Anastomotic leakage; GT: Gastric tube; MINORS: Methodological Index for Non-Randomized Studies; AS: Anastomotic sites; RAMIE: Robotic assisted minimally invasive esophagectomy.

Table 2 Influence of Indocyanine green fluorescence angiography on intraoperative decisions and on anastomotic leakage

Ref.	Entire cohort n = 1186		ICGA study group n = 752		Non ICGA n = 434
		ICGA good perfused AS, n = 592	ICGA good perfused altered AS, n = 93	ICGA poor perfused AS, n = 67
Shimada et al[40]	3/36	2/31	1/5 Superdrainage	-	-
Kubota et al[18]	0/4	0/4	-	-	-
Murawa et al[19]	1/15	1/11	0/4 End-to-end	-	-
Pacheco et al[20]	2/11	1/10	-	1/1	-
Kumagai et al[21]	2/20	2/20	-	-	-
Rino et al[22]	5/33	5/33	-	-	-
Sarkaria et al[23]	2/30	2/30	-	-	-
Hodari et al[25]	3/54	0/39	-	-	3/15
Campbell et al[26]	12/90	0/21	-	-	12/69
Yukaya et al[27]	9/27	9/27	-	-	-
Zehetner et al[28]	24/144	2/95	-	22/49	-
Koyonagi et al[30]	7/40	0/25	-	7/15	-
Schlottmann et al[33]	0/5	0/3	0/2 resection	-	-
Kitagawa et al[29,34]	7/72	3/41 ICG-LMM	0/5 ICG-LMM	-	-
		4/26 ICG	- 0/4 End-to-end
			- 0/1 Superdrainage
Ohi et al[32,35]	10/120	0/50	1/9	-	9/61
			- 0/3 End-to-end
			- 1/1 Supercharge/drain
			- 0/5 Manubriotomy
Karampiris et al[36]	13/90	0/7	1/26 Resection	2/2	10/55
Noma et al[37]	60/285	6/70	0/1 Supercharge/drain	-	54/214
Dalton et al[38]	3/40	0/14	2/6 Resection	-	1/20
Kumagai et al[39]	1/70	0/35	1/35 Resection	-	-

ICGA: Indocyanine green fluorescence angiography.