CURRENT STATUS
Indocyanine Green Fluorescence Angiography and
the Incidence of Anastomotic Leak After Colorectal
Resection for Colorectal Cancer: A Meta-analysis
Renhui Shen, M.D. • Ye Zhang, M.D. • Tong Wang, M.D.
Wuxi People’s Hospital Affiliated to Nanjing Medical University, Wuxi, Jiangsu Province, People’s Republic of China
BACKGROUND:  Anastomotic leak is a life-threatening
complication of colorectal surgery. Recent studies showed
that indocyanine green fluorescence angiography might
be a method to prevent anastomotic leak.
OBJECTIVE:  The purpose of this study was to investigate
whether intraoperative indocyanine green fluorescence
angiography can reduce the incidence of anastomotic leak.
DATA SOURCES:  Potential relevant studies were identified
from the following databases: PubMed, Embase, Web
of Science, Cochrane Library, and China National
Knowledge Infrastructure.
STUDY SELECTION:  This meta-analysis included
comparative studies investigating the association
between indocyanine green fluorescence angiography
and anastomotic leak in patients undergoing
surgery for colorectal cancer where the diagnosis
of anastomotic leak was confirmed by CT and the
outcomes of the indocyanine green group were
compared with a control group.
Funding/Support: This work was supported by grants from the Clini-
cal Medicine Project of Jiangsu Province (BL2014023), National Natural
Science Foundation of China (No.81371683/H1819), Natural Science
Foundation of Jiangsu Province (BK2016198) and National Natural Sci-
ence Foundation of China (No. 81702592).
Financial Disclosure: None reported.
Correspondence: Tong Wang, M.D., Department of General Surgery, Wuxi
People’s Hospital Affiliated to Nanjing Medical University, Wuxi, Jiangsu
Province, 214023 People’s Republic of China. E-mail: aanti@163.com.
Dis Colon Rectum 2018; 61: 1228–1234
DOI: 10.1097/DCR.0000000000001123
Copyright © 2018 The Author(s). Published by Wolters Kluwer Health,
Inc. on behalf of the American Society of Colon and Rectal Surgeons.
This is an open-access article distributed under the terms of the Cre-
ative Commons Attribution-Non Commercial-No Derivatives License
4.0 (CCBY-NC-ND), where it is permissible to download and share the
work provided it is properly cited. The work cannot be changed in any
way or used commercially without permission from the journal.
1228
INTERVENTION:  Indocyanine green was injected
intravenously after the division of the mesentery and
colon but before anastomosis.
MAIN OUTCOME MEASURES:  The Newcastle–Ottawa
Scale was used to assess methodologic quality of
the studies. ORs and 95% CIs were used to assess
the association between indocyanine green and
anastomotic leak.
RESULTS:  In 4 studies with a total sample size of 1177,
comparing the number of anastomotic leaks in the
indocyanine green and control groups, the ORs were
0.45 (95% CI, 0.18–1.12), 0.30 (95% CI, 0.03–2.98),
0.17 (95% CI, 0.01–3.69), and 0.12 (95% CI, 0.03–0.52).
The combined OR was 0.27 (95% CI, 0.13–0.53). The
difference was statistically significant (p < 0.001), and
there was no significant heterogeneity (p = 0.48; I2 = 0).
LIMITATIONS:  Data could not be pooled because of
the small number of studies; some differences between
studies may influence the results. Also, the pooled data
were not randomized.
CONCLUSIONS:  The result revealed that indocyanine
green was associated with a lower anastomotic
leakage rate after colorectal resection. However, larger,
multicentered, high-quality randomized controlled trials
are needed to confirm the benefit of indocyanine green
fluorescence angiography.
KEY WORDS:  Anastomotic leakage; Colorectal cancer;
Fluorescence angiography; Indocyanine green.
C
olorectal cancer is one of the most common
cancers in the world, and the incidence is in-
creasing.1 With novel technical advances, better
understanding of the physiology, and improved surgical
technical skills, surgeons offer patients better outcomes
after colorectal resections, albeit with complications.2
However, among postoperative complications, anasto-
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018)
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018)
motic leakage (AL) is the most serious complication that
has a negative impact on both short- and long-term out-
comes.3 The reported incidence rate of AL after colorec-
tal surgery ranges from 3% to 20%.4,5 Some studies have
suggested that AL is associated with reduced overall sur-
vival and increased rate of local recurrence after resec-
tion for colorectal cancer.3,6
Some investigators have found that poor blood supply
and tension at the anastomotic site are the main risk factors
for AL.7 It has been reported that blood supply is related to
the location of the tumor, preoperative bowel obstruction,
and perioperative transfusion.8 Moreover, absence of Rio-
lan arterial arcade and sacrifice of left colic artery during
resection may also be linked with poor blood supply.9,10
A variety of methods have been used to assess the
anastomotic integrity intraoperatively, including mechan-
ical patency (air leak and dye tests) and endoscopic assess-
ment.11 Meanwhile, several clinical signs, including bowel
serosal color and palpable mesenteric arterial pulsations,
have been used to check the vascularity of the cut end of
the bowel. However, these signs are subjective and may
well lead to misinterpretations even by experienced sur-
geons. Moreover, some of these signs may not be feasible
while performing laparoscopic colon resection.1
Recently, many studies have found that intraoperative
indocyanine green (ICG) fluorescence angiography (ICGFA)
might be useful in preventing AL in colorectal surgery by vi-
sualizing the bowel perfusion of the anastomotic region.12,13
Fluorescence imaging for tissue perfusion assessment has
repeatedly been found to be beneficial in decision-making
and improving surgical outcomes in plastic, cardiothoracic,
hepatobiliary, and foregut surgeries.14–18 Also in colorectal
surgery, ICG fluorescence imaging is useful for assessing
anastomotic perfusion.19 ICG is a sterile, water-soluble tri-
carbocyanine compound that absorbs near infrared light
with a peak spectral absorption at 800 nm. ICG is injected
intravenously, which rapidly and extensively binds to plasma
protein. It can be cleared by the liver in 3 to 5 minutes into
the bile. It is a nontoxic and nonionizing agent with a maxi-
mal daily dose of 2 mg/kg, with few reported cases of adverse
effect.20 There are few systematic reviews and meta-analyses
conducted on the effect of ICGFA in colorectal cancer sur-
geries. Therefore, we aimed to analyze the current evidence
for the impact of intraoperative ICGFA on AL after resection
for colorectal cancer.
MATERIALS AND METHODS
This meta-analysis was carried out in line with the Pre-
ferred Reporting Items for Systematic Reviews and Meta-
Analysis statement.21
1229
Search Strategy
Potential relevant studies were identified by a comprehen-
sive literature search, which covered the following electronic
platforms: PubMed, Embase, Web of Science, Cochrane Li-
brary, and China National Knowledge Infrastructure. The
search was performed independently by 2 researchers, and
no language or date restrictions were applied. The last search
was performed in August 2017. The following terms were
used during literature search: anastomotic leakage, colorectal
cancer, fluorescence angiography, fluorescence imaging, and
indocyanine green. The reference lists of all retrieved articles
were screened to identify other relevant studies.
Selection Criteria
Studies satisfying the following criteria were included in
the meta-analysis: 1) comparative studies investigated
the association between ICGFA and AL in patients un-
dergoing surgery for colorectal cancer, 2) the diagnosis
of AL was confirmed via CT, and 3) the outcomes of the
study cohort undergoing ICGFA were compared with a
control group in which ICGFA was not performed. Ex-
clusion criteria were publication types such as case re-
ports, letters reviews, meeting abstracts, meta-analyses,
and proceedings, as well as studies lacking necessary data
for calculation.
Data Extraction and Study Quality
Data were extracted by 1 investigator with complete and in-
dependent verification by another investigator. Each of the
2 reviewers assessed the studies independently based on the
selection criteria to collect the following descriptive infor-
mation from eligible studies: surname and initials of the first
author, year of publication, journal, country where study
was conducted, study design, number of subjects, type of op-
eration, cancer type, demographic variables of the patients,
ICG dose, and postoperative complications. Discrepancies
between the 2 investigators were settled by discussion. Be-
cause of the mix of randomized controlled trials (RCTs) and
cohort studies, risk of bias and qualities of included studies
were assessed using the Newcastle–Ottawa Scale.22 Studies
with a score of ≥7 were considered high quality.
Statistical Analysis
All of the statistical analyses were performed with Review
Manager 5.1 (The Cochrane Collaboration, The Nordic
Cochrane Centre, Copenhagen, Denmark). The ORs and
95% CIs were used as the statistical measures for dichoto-
mous outcomes to calculate the relevance of ICGAF and
the incidence of AL after colorectal cancer. ORs were calcu-
lated from the original data and combined with the Man-
tel–Haenszel method. OR > 1.0 indicated greater risk of an
adverse event in the experimental group. A p < 0.05 was
considered significant for all of the analyses. Heterogeneity
among studies was tested using χ2 and I2 statistics and the
1230 SHEN ET AL: ICGFA AND AL AFTER COLORECTAL RESECTION

Identification Records identified through Additional records identified

database searching through other sources
(n = 148) (n = 0)

Records after duplicates removed

(n = 67)
Screening

Records excluded on basis of abstract/title

(n = 23):
Records screened
(n = 14): case reports, reviews,
(n = 67)
conference abstracts
(n = 9): not related to research topics

Full-text articles assessed

for eligibility Full-text articles excluded
Eligibility

(n = 44) (n = 39):
(n = 36): not case-control study
(n = 3): lack necessary data

Studies included in
qualitative synthesis
(n = 5)
Included

Studies included in
quantitative synthesis
(meta-analysis)
(n = 4)

FIGURE 1.  Flow diagram depicting the process of selection of studies for the meta-analysis.

funnel plot. A p < 0.05 and I2 > 50% indicate significant
heterogeneity. In these cases, a random-effects model was
used; otherwise a fixed-effect meta-analysis was performed.
RESULTS
Description of Included Studies
A total of 148 records were identified on initial searching.
After the exclusion of 81 duplicated studies, the remain-
ing studies (n = 67) were screened by title and abstract
for relevance. Twenty-three studies were excluded because
these were case reports, reviews, or conference abstracts
(n = 14) or not related to research topics (n = 9). Full texts
of the remaining 44 records were retrieved and evaluated.
Among these 44 studies, 39 studies were unsuitable be-
cause of a lack of control group (n = 36) or necessary data
(n = 3). In addition, among the included 5 studies, 1 study
was excluded because the same patients were included in
another recent study by the same authors.23,24 Finally, 4

TABLE 1.   Basic information of included studies

No. Sex NOS
Study Year Country of patients (men/women) Cancer type Operation method scorea
Kim et al24 2017 Korea 657 398/259 Rectal cancer Robot-LAR 8
Kudszus et al25 2010 Germany 402 170/232 Colorectal cancer L/C 7
Jafari et al26 2013 United States 38 28/10 Rectal cancer Robot-LAR 6
Boni et al27 2016 Italy 80 50/30 Rectal cancer L-LAR 7
LAR = low anterior resection; L = laparoscopic; C = conventional.
a
Data were calculated using the Newcastle–Ottawa Scale (NOS) for assessment of the quality of nonrandomized studies in meta-analyses.22
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018) 1231

ICGFA Control OR OR
Study or subgroup Events Total Events Total Weight M-H, Fixed, 95% CI Year M-H, Fixed, 95% CI
Kudszus et al25 7 201 15 201 39.0% 0.45 (0.18—1.12) 2010
Jafari et al26 1 16 4 22 8.5% 0.30 (0.03—2.98) 2013
Boni et al27 0 42 2 38 7.0% 0.17 (0.01—3.69) 2016
Kim et al24 2 310 18 347 45.5% 0.12 (0.03—0.52) 2017

Total (95% CI) 569 608 100.0% 0.27 (0.13—0.53)

Total events 10 39
Heterogeneity: χ2 = 2.48, df = 3 (p = 0.48); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: z = 3.72 (p = 0.0002)
Favors (ICGFA) Favors (control)

FIGURE 2.  Forest plot analysis. df = degrees of freedom. ICGFA = indocyanine green fluorescence angiography; MH = Mantel–Haenszel
method.

retrospective case–control studies published from 2010 to
2017 were incorporated into the current meta-analysis.24–27
A flow diagram of study selection is displayed in Figure 1.
The included 4 studies were from 4 different coun-
tries with a total sample size of 1177 patients, and all of
the studies divided samples into ICGFA group and control
group. All 4 studies were retrospective case-matched and
single-institutional studies with the primary end points
being the incidence of AL requiring surgical reinterven-
tion and change in the surgical strategy. Three studies
investigated patients with rectal cancer,24,26,27 and 1 study
investigated patients with colorectal cancer.25 Moreover,
the operation method differed among the studies: in 2
studies surgeries were performed by robot-assisted laparo-
scopic method,24,26 whereas in the other studies surgeries
were conducted by laparoscopic/conventional method.25,27
Table 1 shows the baseline characteristics of included
studies. Two studies mentioned the use of diversion: in
the study by Jafari et al,26 the rate of diversion was 75%
in the ICG group and 77% in the control group, where
the decision to use diversion was left to the discretion of
the attending surgeon; in another study,24 concurrent il-
eal diversion was performed in patients with preoperative
SE (log[OR])
0 sults were statistically reliable.
chemoradiotherapy or a complicated operation, including
coloanal anastomosis or inadequate perfusion.
ICGFA and AL After Operation of Colorectal Cancer
This meta-analysis found that the use of intraoperative IC-
GFA was associated with lower incidence of AL after sur-
gery for colorectal cancer (Fig. 2). Among the 4 studies, the
main outcomes were 4.0% overall reduction in leak rate
and 16.4% change in surgical plan,25 12.0% overall reduc-
tion in leak rate and 19.0% change in resection margins,26
5.0% overall reduction in leak rate and 4.7% change in sur-
gical plan,27 and 4.9% overall reduction in leak rate.24 The
corresponding OR values were 0.45 (95% CI, 0.18–1.12),
0.30 (95% CI, 0.03–2.98), 0.17 (95% CI, 0.01–3.69), and
0.12 (95% CI, 0.03–0.52). The combined OR value was
0.27 (95% CI, 0.13–0.53). The result revealed that ICGFA
was associated with a lower AL rate after colorectal resec-
tion. The difference was statistically significant (p < 0.001),
and there was no significant heterogeneity (χ2 = 2.48;
degrees of freedom = 3; p = 0.48; I2 = 0).
Publication Bias
From the funnel plot (Fig. 3), the included studies were of
symmetrical distribution, and the p value for the Egger test
was 0.373. Both demonstrated that there was no evidence
of significant bias in this meta-analysis; therefore, our re-

0.5 DISCUSSION
This meta-analysis found that use of ICGFA was associ-
1.0
ated with a lower AL rate after colorectal resection. Thus,
we conclude that intraoperative ICGFA has a link with a
lower AL rate of colorectal cancer surgery. The lower AL
1.5 rate is probably attributed to better assessment of bowel
perfusion and vascularity with the help of ICG. Moreover,
ICGFA changed the surgical plan by guiding the appropri-
2.0 ate line of bowel transection in 4.7% to 19.0% of cases.25–27
0.01 0.1 1 10 100 Recently, fluorescence angiography using ICG has
OR
become the most promising technology that allows for
FIGURE 3.  Funnel plot diagram. real-time intraoperative objective evaluation of bowel per-
1232 SHEN ET AL: ICGFA AND AL AFTER COLORECTAL RESECTION

fusion.13,26,28 A review by Mizrahi and Wexner29 pointed out

that every surgeon needs to become familiar with methods

12.0% overall reduction in

leak rate; 16.4% change

leak rate; 19.0% change

4.9% overall reduction in

4.0% overall reduction in

5.0% overall reduction in

leak rate; 4.7% change
of using ICG and its numerous clinically important ap-

in resection margins
Main outcomes

plications.29 A systematic review about near-infrared fluo-

in surgical plan

in surgical plan
rescence (NIRF) angiography in anastomotic colorectal
surgery for cancers, diverticulitis, and Crohn's disease con-
leak rate

cluded that 3.5% (31 of 894) of all NIRF patients and 7.4%
(32 of 434) of all control patients developed an anastomot-
ic leakage (p=0.002).30 Another meta-analysis including 5
in surgical

studies concluded the similar result,31 but the surgical indi-

Change

plan, %

16.4

19.0

4.7
NS

cation of one included study was not only cancer but also
IBD and diverticular disease.32 The results of non-colorec-
tal cancer surgery may affect the final statistics. In addition,
Leak rate, %

Control: 18.0

it included a study that may be outdated that we mention

Control: 5.5

6.8 min Control: 7.5

Control: 5

in the "Description of Included Studies" section.23,24 There-

ICG: 0.6

0.2-0.5 mg/kg Additional ICG: 3.5

ICG: 6.0

ICG: 0

fore, we performed the current meta-analysis to investigate

the correlation between intraoperative ICGFA and the AL
rate after colorectal resection for colorectal cancer. All 4 of
Time
NS

NS

NS

the studies showed that ICGFA reduced the AL rate after

colorectal resection. Because the difference in AL rate was
statistically significant with no significant heterogeneity or
ICG dose

bias, it is clear that ICGFA was related to a lower AL rate af-

0.2 mg/kg
6-8 mg

ter colorectal resection. We have also tried to perform some

10 mg

similar operations with the use of ICG. However, because

of several technological limitations and insufficient sample
Pulsion Medical Systems,

(Karl Storz, Tuttlingen,

angiography (IC-View,

size, our results were not as robust as the results of recent

Intuitive Surgical Inc)
Intuitive Surgical Inc,
angiography (Firefly,

angiography (Firefly,

fluorescence system
Camera system

studies. Despite this we estimated that the reduction rate

Rastatt, Germany)
Laser-assisted ICG

Laser-assisted ICG

Laser-assisted ICG

Karl Storz image1

of AL in our clinical trials was ≈4% to 6%. However, there

Sunnyvale, CA)

were differences in the included studies. Table 2 shows the

Germany)
ICG = Indocyanine green; LAR = low anterior resection; L = laparoscopic; C = conventional; NS = not stated.

detailed characteristics of these studies.

With the development of surgical techniques, many
surgeries for colorectal cancer are being increasingly per-
formed by laparoscopic and robot-assisted methods. Stud-
(average), cm
Anastomotic

Control: 5.9

Control: 7.2

ies have found good long-term results with laparoscopic

level

ICG: 5.4

ICG: 6.3

colorectal resection for colorectal cancer.33,34 On the oth-

er hand, robotic-assisted laparoscopic surgery also has
5.5
NS

shown some advantages over open surgery.35,36 However,

Surgical approach

colectomy: 63
and procedure

there was no difference between laparoscopic and robot-

and LAR: 131
Left colectomy

assisted resection in terms of postoperative AL rate.37,38

Robot-LAR

Robot-LAR
L/C right
TABLE 2.   Detailed information of included studies

Therefore, we believe that the type of operation is unlikely

L-LAR

to affect the results of this meta-analysis. Similarly, other

factors like patient demographic and preoperative charac-
teristics were considered to have no significant differences.
398/259

170/232
women)

28/10

50/30
(men/
Sex

Several limitations in this meta-analysis should be

mentioned. First, we did not take unpublished articles and
abstracts into account because the necessary data were
Control: 347

Control: 201

Control: 22

Control: 38

lacking. A second potential limitation was that, among the

ICG: 310

Kudszus et al25 ICG: 201

4 studies, the administered dose of intraoperative ICG and

ICG: 16

ICG: 42
n

camera systems were different, and whether the different

doses would influence the results needs to be confirmed.
Also, this limitation may introduce a little heterogeneity.
Jafari et al26

Boni et al27
24

Last but not least, this meta-analysis did not include RCTs,
Kim et al

and the pooled data were not randomized. Accordingly,

Study

larger, multicenter, high-quality RCTs are needed to verify

the findings of this meta-analysis.
DISEASES OF THE COLON & RECTUM VOLUME 61: 10 (2018)
CONCLUSION
This meta-analysis showed significant benefit of ICGFA in
reducing the incidence of AL, thereby improving patient
outcomes. In the long term, it may offer the possibility to
lower the rate of mortality, as well as more promising ad-
vantages, such as lymph node evaluation.
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